Significance The vestibular system provides a critical role to coordinate balance and movement, yet it remains an underappreciated sense. Functional MRI (fMRI) reveals much information about brain-wide sensory and cognitive processes. However, fMRI mapping of regions that actively process vestibular information remains technically challenging, as it can permit only limited movement during scanning. Here, we deploy fMRI and optogenetic stimulation of vestibular excitatory neurons to visualize numerous brain-wide central vestibular pathways and interrogate their functional roles in multisensory processing. Our study highlights multiple routes to investigate vestibular functions and their integration with other sensory systems. We reveal a method to gain critical knowledge into this critical brain system.