Organization and remodeling of the olivocerebellar climbing fiber projection

Climbing fibers, terminal portions of the axons of inferior olive neurons, form strong synaptic connections to Purkinje cells in an exclusive one-to-one relationship. This projection is established during development by drastic reshaping in each climbing fiber and in overall axonal arborization. Early climbing fibers form loose 'creeper'-type terminal arbors that seem to make weak contact with many Purkinje cells in the first postnatal week. The terminal arbor then becomes focused on a single Purkinje cell with the aggregation of swellings ('transitional' type), and eventually tightly surrounds the Purkinje cell soma ('nest' type) in the second postnatal week. The terminal arbor is then displaced upward to the stem of the apical dendrite of the Purkinje cell ('capuchon' or 'hood') and eventually to the proximal portion of the dendritic tree (mature climbing fiber). Single-axon morphology in rats has shown that olivocerebellar axons in the creeper stage branch more frequently and have many more climbing fibers than those in adults. The climbing fibers that originate from an axon are largely organized into microzones as in adults. Concomitant with this remodeling of climbing fibers, the number of climbing fibers per olivocerebellar axon is significantly decreased by the putative retraction of climbing fibers during development from the creeper to nest stage. Due to additional retraction after the nest stage, an olivocerebellar axon in an adult has about seven climbing fibers. The above morphological remodeling and retraction during development can be closely compared to the changes in climbing fiber-Purkinje cell synaptic interaction observed in rats and mice. Generation and aggregation of the swellings in the terminal arbor between the creeper and nest stages are correlated with maturation of the synaptic connection. The decrease in climbing fibers in the same and following periods is correlated with the elimination of overabundant synapses to establish one-to-one connections.