Acquisition of new repertoire requires reorganization of existing brain networks, which are enhanced and maintained by active and prolonged interaction between organisms and external environments. We developed a step-by-step protocol to train common marmosets to retrieve a food item by using a rake-shaped tool, and found that it took almost one year of training to acquire this new skill. Then we investigated volumetric changes in the brain structure of the trained marmosets as they learnt to use tool. We performed structural MRI scans before, during, and after the training, and confirmed that long term tool use training induced volumetric changes in several brain structures which clearly differed from those of short term training. The volume of nucleus accumbens increased in the later phases of the training, and was positively correlated with performance indices, but not with the number of reinforcers earned, suggesting increased motivation for tool use as marmosets effectively learned to use the rake. Other brain regions also increased volume including visual areas, STS, and the anterior trunk of the corpus callosum. White matter changes also occurred in the middle and inferior cerebellar peduncles which could reflect the sustained capacity for tool use long after completion of training. These unique brain areas supported gradual but drastic behavioral and motivational changes during long-term training, both for acquisition and maintenance of a novel skill. (This work was supported by the Funding Program for World-leading Innovative R&D on Science and Technology (FIRST) at RIKEN, Japan)