Acoustic short tone bursts (STB) trigger ocular and cervical vestibular-evoked myogenic potentials (oVEMPs/cVEMPs) by activating irregular otolith afferents. Simultaneously, STBs introduce an artificial net acceleration signal of otolith origin into the vestibular network. VEMP parameters as diagnostic otolith processing markers have been shown to decline after the age of thirty. To delineate the differential effects of healthy ageing on the cortical vestibular subnetwork processing otolith information, we measured cVEMPs and the differential effects of unilateral STB in three age groups (20-40, 40-60 and 60+; n = 42) using functional neuroimaging. STB evoked responses in the main vestibular hubs in the parieto-opercular cortex. Whereas cVEMP amplitudes declined linearly with age, analysis of the BOLD response size depicted a u-shaped curve. Vestibular perception of the otolith stimulus on the other hand remained unchanged with age. Therefore, we propose that the comparably larger BOLD responses past the age of sixty could reflect a mechanism of central sensitisation for otolith perception to counterbalance the concurrent peripheral vestibular and somatosensory function decline.