Functional architecture of vestibular primary afferents from the posterior semicircular canal of a turtle, Pseudemys (Trachemys) scripta elegans

Abstract

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.

Regeneration of Vestibular Otolith Afferents after Ototoxic Damage

“…Salient to the present findings, a brief review of the afferent terminal morphologies innervating the pigeon otolith maculas is provided. As shown in Figure 1, birds have three classes of terminal innervation patterns for vestibular afferents, as in all amniote vertebrates (Ramon y Cajal, 1909;Lorente de Nó , 1926;Fernandez et al, 1988Fernandez et al, , 1990Fernandez et al, , 1995Schessel et al, 1991;Brichta and Peterson, 1994;Si et al, 2003;Zakir et al, 2003). Calyx units innervate type I hair cells with a calyceal terminal that encloses one or several hair cells, with small terminal fields (Fig.…”

Mechanisms of Efferent-Mediated Responses in the Turtle Posterior Crista

“…There are four populations of afferents having distinctive locations in each hemicrista (Brichta and Peterson, 1994;Brichta and Goldberg, 2000a) (Fig. 1 J).…”

Recovery of Gaze Stability During Vestibular Regeneration

“…However, these calyceal terminals were rudimentary and were exclusively located on simple dimorph afferents (fibers that contain both calyceal and bouton terminals), as calyx afferents (containing exclusive calyceal terminals) did not yet exist (Zakir and Dickman 2006). Early stage 2 regeneration was also marked by the lack of significant numbers of hair cells or afferents in the central regions of the receptor epithelia, areas known to contain the highest density of type I hair cells and calyceal terminalbearing afferents (Brichta and Peterson 1994;Haque et al 2006;Lysakowski and Goldberg 1997;Si et al 2003;Zakir et al 2003). Here gaze responses exhibited increasing gains, particularly in the mid-to high-frequency range, although the lowest frequencies tested (0.01 and 0.02 Hz) still produced little compensatory response.…”