Coordinated neuronal population activity is essential for brain function, yet how such network-level organization emerges during development remains incompletely understood. Here, we conducted whole-cerebellar calcium imaging at cellular scale in zebrafish larvae to investigate the developmental maturation of Purkinje cell population dynamics. Visual stimulation evoked large, spatially organized Purkinje cell clusters driven by inferior olive inputs and accompanied by coherent optokinetic behavior. In the absence of stimuli, Purkinje cells formed transient assemblies exhibiting distance-dependent coordination. During development, long-range coordination progressively emerged, transforming locally correlated activity into distributed cerebellar population dynamics. Early enucleation, but not dark rearing, disrupted this developmental acquisition of long-range coordination and induced aberrant population clustering, indicating a retina-dependent mechanism underlying cerebellar network formation. Together, our findings reveal key organizational features underlying the developmental emergence of coordinated cerebellar population dynamics and suggest that early retina-dependent signals shape population-level organization.
Hiyoshi, K., Miyanari, K., Okuda, E., Fukuda, N., Saito, K., Murayama, T., Kawamura, R., Matsuzaki, T., Yoshikawa, H. Y., Hibi, M., Tsuda, S.
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