Functional architecture of vestibular primary afferents from the posterior semicircular canal of a turtle, Pseudemys...

Physiological studies in many vertebrates indicate that vestibular primary afferents are not a homogeneous population. Such data raise the question of what structural mechanisms underlie these physiological differences and what functional role is played by afferents of each type. We have begun to answer these questions by characterizing the architecture of 110 afferents innervating the posterior canal of Pseudemys scripta. We emphasize their spatial organization because experimental evidence suggests that afferent physiological properties exhibit significant spatial heterogeneity. The sensory surface of the posterior canal comprises paired, triangular hemicristae, which are innervated by two afferent types. Bouton afferents (66% of total afferents) are found over the entire sensory surface. They differ significantly in the shape and size of their collecting areas, number of boutons, soma size, and axon diameter; this morphological variation is systematically related to the afferent's spatial position. In addition, multivariate analyses suggest that bouton afferents may comprise two subtypes: alpha afferents have delicate processes and are found throughout the crista; beta afferents are more robust and are concentrated preferentially toward the canal center. Calyx-bearing afferents comprise two morphological subtypes: dimorphs (13% of total afferents) bear calyceal and bouton endings; calyceal afferents (21%) bear calyceal endings only. Both types occur exclusively in an elliptical region near the center of each hemicrista; their morphology varies with radial distance from the center of this elliptical region. Our data provide evidence that in Pseudemys: (1) the classical vestibular afferent types (bouton, calyx, dimorph) are structurally heterogeneous, and (2) their spatial sampling characteristics are highly structured and distinctive for each type. These spatial patterns may shed light on regional differences in physiological profiles of vestibular afferents, and they raise questions about the role of this spatial heterogeneity in signaling head movement.