The cerebellum is involved not only in motor coordination, training, and memory, but also in cognition and emotion. Lobule VI in particular belongs to sensorimotor, salience, and executive cerebellar networks. This study aims to determine whether lobule VI would constitute an integrative interface between motor and cognitive/emotional circuits during a motor task with verbal encouragement, likely in conjunction with the basal ganglia (reward and motivational system). We used fMRI to identify specific recruitment of cerebellar and striatal systems during physical performance using two motor tasks with and without encouragement. We found that: (i) Force results were higher during verbal encouragement than during basal condition in all participants. (ii) The anterior part of the right lobule VI was activated by motor execution in both tasks, while its posterior part was specifically activated by verbal encouragement. (iii) The closed-connectivity loop maintained motivation induced by verbal encouragement between cerebral and cerebellar through the red nucleus and striatal network. Therefore, right lobule VI is a hub-controlling sensorimotor and motivates aspects of motor performance in relation with the red nucleus and the ventral striatum. These results could have important implications for extrapyramidal and multisystem degenerative diseases.