The brain’s remarkable ability to respond rapidly and adaptively to self-motion signals in everyday life relies on signal processing in the vestibular system. Neurons in the brainstem vestibular nuclei that transform inner ear signals into appropriate motor commands have long been modeled as generic linear operators with little attention to underlying cell biology. Our studies of intrinsic and synaptic physiology and of differential gene expression indicate, to the contrary, that vestibular nucleus neurons are biophysically specialized for their distinct roles in behavioral signal processing. Coordinated expression of ion channel genes produces gradient of cell types differentially tuned for precise spike timing vs subthreshold integration. Vestibular neurons with distinct physiological personalities are thus differentially responsible for rapid initiation vs maintained stability of vestibular behaviors.