The critical maturation time of central otolith neurons in processing spatial orientations was examined in Sprague-Dawley rats. With the use of immuno-hybridization histochemical methods, we observed c-fos expression in vestibular nuclear neurons responding to transverse movement on the horizontal plane as early as P7 and those to antero-posterior stimulation as early as P9. In the inferior olive (IO) sub nuclei, downstream relays of the vestibulo-olivary pathway, c-fos expression was not observed until P11-13. These findings reveal a difference in critical maturation time between relays of the vestibulo-olivary pathway in the recognition of gravity-related horizontal orientations. Central recognition of vertical orientations also showed different critical maturation time between relay stations. Besides, progressive changes in resting and spatio-temporal neuronal properties as well as the expression of NMDA and AMPA receptor subunits on these otolith-related neurons were observed with age. We examined if otolith information along the horizontal plane is topographically represented in the vestibulo-olivary pathway. Our in vivo electrophysiological results demonstrated that the best response vectors of otolith-related vestibular nuclear neurons in P7 rats were restricted to the interaural axis while those of adults were multi-directional on the horizontal plane. Based on results from both approaches, we found that neurons differing in response vectors were randomly distributed in different vestibular subnuclei without any apparent topographic pattern. Evidence of a gravity-related topographic spatial organization was however observed in sub nuclei of the IO (viz. DMCC, IO) along its rostrocaudal dimension. Although neurons in the caudal IO displayed the adult topographic response pattern to antero-posterior movement as early as P13, those responsive to transverse movement progressively declined from P13 to adulthood. In contrast, neurons in the rostral IO progressively showed the adult pattern to movements in both directions by the third postnatal week. Taken together, these results reveal refinement of topography in the postnatal IO as a model for mapping the establishment of functional synaptic inputs in a plastic stage of growing axons.