Population activity of mossy fibre axon input to the cerebellar cortex during behaviours

The cerebellum gathers information from the neocortex via the cortico-ponto-cerebellar pathway, and forms sensorimotor associations for predicting movements and their sensory consequences. However, little is known about the functional properties of this major input to the cerebellar cortex. Recordings from individual cerebellar mossy fibre axons (MFAs) have shown that they convey sensory and motor information, but nothing is known about their population code. Here, we report that the population activity of pontine MFAs is heterogeneous, high-dimensional and that different subpopulations of MFAs are active during quiet and active behavioural states. Population activity occupied a substantial fraction of the state space and some MFAs are particularly informative about behaviour. Surprisingly, positively and negatively modulated MFAs are intermingled, suggesting granule cells integrate opposite-signed inputs to generate mixed bidirectional sensorimotor representations. Our results establish that neocortex and cerebellum can communicate with a low redundancy, high capacity, bidirectional population code, which is well-suited for forming sensorimotor associations.