Cerebellar granule cell axons support high dimensional representations

In classical theories of cerebellar cortex, high dimensional sensorimotor representations are used to separate neuronal activity patterns, improving associative learning and motor performance. Recent experimental studies suggest that cerebellar granule cell (GrC) population activity is low dimensional. To examine sensorimotor representations from the point-of-view of downstream Purkinje cell ‘decoders’, we used 3D acousto-optic lens two photon microscopy to record from hundreds of GrC axons. Here we show that GrC axon population activity is high dimensional and distributed with little fine-scale spatial structure during spontaneous behaviors. Moreover, distinct behavioral states are represented along orthogonal dimensions in neuronal activity space. These results suggest that the cerebellar cortex supports high dimensional representations and segregates behavioral state dependent computations into orthogonal subspaces, as reported in the neocortex. Our findings match the predictions of cerebellar pattern separation theories and suggest that the cerebellum and neocortex utilize population codes with common features, despite their vastly different circuit structures.