Population-scale organization of cerebellar granule neuron signaling during a visuomotor behavior

ABSTRACTGranule cells at the input layer of the cerebellum comprise over half the neurons in the human brain and are thought to be critical for learning. However, little is known about granule neuron signaling at the population scale during behavior. We used calcium imaging in awake zebrafish during optokinetic behavior to record transgenically identified granule neurons throughout a cerebellar population. A significant fraction of the population was responsive at any given time. In contrast to core precerebellar populations, granule neuron responses were relatively heterogeneous, with variation in the degree of rectification and the balance of excitation versus inhibition. Functional correlations were strongest for nearby cells, with weak spatial gradients in the degree of rectification and excitation. These data open a new window upon cerebellar function and suggest granule layer signals represent elementary building blocks underrepresented in core sensorimotor pathways, thereby enabling the construction of novel patterns of activity for learning.SIGNIFICANCE STATEMENTCerebellar processing is important for a variety of fine motor tasks and sensorimotor adaptations, and a growing body of evidence indicates a prominent role in cognitive control. However, it has been challenging to understand cerebellar function during behavior because of difficulties in recording from cerebellar granule neurons, the most populous neuron type in the brain. We use population-scale optical imaging in the larval zebrafish to compare precerebellar activity to granule cell signaling. Our results suggest a behaviorally relevant expansion of precerebellar signaling representations at the granule layer of the cerebellum.