The utricle provides critical information about spatiotemporal properties of head movement. It comprises multiple subdivisions whose functional roles are poorly understood. We previously identified four subdivisions in turtle utricle, based on hair bundle structure and mechanics, otoconial membrane structure and hair bundle coupling, and immunoreactivity to calcium-binding proteins. Here we ask whether these macular subdivisions are innervated by distinctive populations of afferents to help us understand the role each subdivision plays in signaling head movements. We quantified the morphology of 173 afferents and identified six afferent classes, which differ in structure and macular locus. Calyceal and dimorphic afferents innervate one striolar band. Bouton afferents innervate a second striolar band; they have elongated terminals and the thickest processes and axons of all bouton units. Bouton afferents in lateral (LES) and medial (MES) extrastriolae have small-diameter axons but differ in collecting area, bouton number, and hair cell contacts (LES ϾϾ MES). A fourth, distinctive population of bouton afferents supplies the juxtastriola. These results, combined with our earlier findings on utricular hair cells and the otoconial membrane, suggest the hypotheses that MES and calyceal afferents encode head movement direction with high spatial resolution and that MES afferents are well suited to signal three-dimensional head orientation and striolar afferents to signal head movement onset. hair cells; turtle; utricle; vestibular afferents THE VESTIBULAR LABYRINTH is poorly understood compared, for example, to the auditory periphery and the retina. This is especially true of the major otoconial organs, the utricle and saccule, which encode linear head accelerations, including head position in gravity space, and transmit this information to the CNS. One important question is how the sensory surface of otoconial organs is organized to transduce the full range of signals generated by head movement. There are two broad possibilities: 1) all regions are equipotential in their ability to encode temporal properties of head movement (e.g., different frequencies, accelerations) or 2) different regions of the macula play distinctive functional roles.Considerable evidence supports the second of these alternatives. The best-known example of regional specializations in otoconial maculae is the ubiquitous division between striola and extrastriola: the striolar region of vertebrate maculae differs from the extrastriola in the structure and molecular composition of the otoconial membrane (OM) (e.g., Goodyear et al. 1994;Lim 1979;Lindeman 1969;Werner 1933; reviewed in Fermin et al. 1998;Lewis et al. 1985), which transmits the mechanical stimuli arising from head movements to receptors (hair cells), and in the structure and physiology of its hair cells (e.g