Competitive Olivocerebellar Input Selection Promotes Resilient Circuit Formation

Abstract

Many neural circuits undergo competitive input selection, a process in which supernumerary connections compete for innervation territory on target cells. This process can create atypical circuits when functional inputs are favored over compromised ones. Yet, it is often unclear whether such atypical circuits are maladaptive or promote functional resilience. We investigated this using the olivocerebellar climbing fiber circuit, where multiple inputs compete to mono-innervate Purkinje cells. We found that eliminating neurotransmission from [~]50% of olivocerebellar neurons reduced climbing fibers competitiveness during input selection and decreased survival of parental inferior olive neurons. Conversely, functional climbing fibers expanded their innervation territory. Despite these atypical circuits, climbing-fiber-dependent motor control was only minimally affected and social behaviors were fully preserved. These results demonstrate that neurotransmission-dependent competition promotes resilient circuits formation, maintaining complex behaviors even when a large proportion of inputs to the cerebellum are developmentally compromised.