Comparing the Representation of a Simple Visual Stimulus across the Cerebellar Network

Abstract

The cerebellum is a conserved structure of the vertebrate brain involved in the timing and calibration of movements. 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 instruct 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 IONs and GCs responses to flashes of diverse luminance and duration. First, we observe that GCs show tonic and graded responses, as opposed to IONs, whose activity peaks mostly at luminance transitions, consistently 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 exhibit sustained responses for the entire duration of the stimulus, while in others activity ramps up with slow time constants. This activity could provide a substrate for time representation in the cerebellum. 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.Significance statementThe cerebellum is an important brain structure shared by all vertebrates, playing a crucial role in sensorimotor behavior. By using calcium imaging in larval zebrafish, we investigated sensory responses across granule cells (GCs), Purkinje cells. (PCs), and inferior olive neurons (IONs). We describe how GCs show tonic and graded responses, as opposed to IONs, more active at stimulus transition times, confirming the notion that GCs and IONs encode context and error information, respectively. We also show how time could be represented in the cerebellum by patterned activity in GCs. Together, our observations 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.