Most animals are born with a minimal repertoire of behaviors, which is gradually expanded as they grow and adapt to their changing needs, environments, and body morphology. The emergence of new functional capacities is associated with changes in the brain architecture, as new neurons become functional and new connections are formed. How brain maturation orchestrates phenotypic transformations during development is still an open question in behavioral neuroscience. Here, we investigate this question in Danionella cerebrum, a novel vertebrate model whose brain remains small and transparent up to the adult stage, thus offering a unique opportunity to perform large-scale monitoring of brain activity with cellular resolution through its entire lifespan.A customized freely-swimming assay was developed to obtain a comprehensive dataset on exploratory behavior throughout development. This setup enables the examination of swimming kinematics with high spatial resolution and across various time scales. On the short timescale of seconds, hydrodynamic arguments are employed to elucidate the behavioral ontogeny by establishing a connection between phenotypic changes in behavior and morphologic growth. On a longer timescale, spanning tens of minutes, a Markovian-based state space model is utilized to uncover the inherent structure of exploration, consistently maintaining a cross-age comparative perspective. Finally, calcium imaging across development will elucidate the functional role of neuronal circuits underlying this phenotypic transition. Our ultimate objective is to present a comprehensive overview of circuit maturation affecting locomotion.