Comparing the representation of a simple visual stimulus across the cerebellar network

The cerebellum is a highly conserved structure of the vertebrate central nervous system that plays a role in the timing and calibration of motor sequences. Its function is supported by the convergence of fibers from granule cells (GCs) and inferior olive neurons (IONs) onto Purkinje cells (PCs). Theories of cerebellar function postulate that IONs convey error signals to PCs that, paired with the contextual information provided by GCs, can be used as a teaching signal to guide motor learning. Here, we use the larval zebrafish to investigate (i) how sensory representations of the same stimulus vary across GCs and IONs and (ii) how PC activity reflects these two different input streams. We use population calcium imaging to measure the cell responses to flashes of diverse luminance and duration to show that IONs and GCs encode different stimulus properties. First, most GCs show tonic and graded responses, as opposed to IONs, whose activity peaks only at on and off luminance transitions, in agreement with the notion that GCs and IONs encode context and error information, respectively. Secondly, we show that GC activity is patterned over time: some neurons had sustained responses for the entire duration of the stimulus, while in others activity was ramping up with slow time constants. This suggests that, by performing temporal integration, GCs could provide a basis that PCs may use to decode time. Finally, we show how PC activity can be largely reconstructed by a linear combination of granule cells and inferior olive neurons. Together, our observations give support to the notion of an error signal coming from IONs, and provide the first experimental evidence for a temporal patterning of GC activity over many seconds.