Synaptic organization of tooth pulp afferent terminals in the rat trigeminal sensory nuclei

Abstract

Previous studies provide evidence that a structure/function correlation exists in the distinct zones of the trigeminal sensory nuclei. To evaluate this relationship, we examined the ultrastructure of afferent terminals from the tooth pulp in the rat trigeminal sensory nuclei: the principalis (Vp), the dorsomedial part of oral nucleus (Vdm), and the superficial layers of caudalis (Vc), by using transganglionic transport of wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP). A total of 93 labeled boutons were serially sectioned, in which some sections were incubated with gamma-aminobutyric acid (GABA) antiserum. Almost all labeled boutons formed asymmetric contact with nonprimary dendrites, in which more than half of labeled boutons in the Vc made synapses with their spines. The labeled boutons could be divided into two types on the basis of numbers of dense-cored vesicles (DCVs) in a boutons: S-type and DCV-type. Almost all labeled boutons in the Vp and Vdm were S-type, whereas two types were distributed evenly in the Vc. In contrast to DCV-type boutons, the S-type was frequently postsynaptic to unlabeled axon terminals containing a mixture of round, oval, and flattened vesicles (p-endings) and forming symmetrical synapses. Most p-endings examined were immunoreactive to GABA. The frequency of axoaxonic contacts was higher for labeled boutons in the Vp than in the Vdm and Vc. These results suggest that the three structures of trigeminal sensory nuclei serve distinct functions in nociceptive processing.

Ultrastructural analysis of the synaptic connectivity of TRPV1‐expressing primary afferent terminals in the rat trigeminal caudal nucleus

“…About 42% of TRPV1+ terminals made synaptic contacts with dendritic spines, and dendritic spines constituted ∼30% of the postsynaptic elements of the TRPV1+ terminals. We found previously that terminals of oral nociceptive afferents make synaptic contacts with dendritic spines far more frequently in the Vc than in other trigeminal sensory nuclei (Bae et al, 2003). Vc is the principal relay nucleus for the nociceptive primary afferents from orofacial regions.…”

“…This is analogous to the pattern of termination of peptidergic C fiber terminals, most of which rarely participate in synaptic glomeruli in the spinal dorsal horn (Barber et al, 1979; Carlton et al, 1988; McNeill et al, 1988; Alvarez et al, 1993). In contrast, the majority of tooth pulp afferent terminals, which arise mainly from small myelinated Aδ fibers, participate in complex synaptic arrangements in the Vc (Bae et al, 2003; Paik et al, 2009), similar to the terminals of Aδ high‐threshold mechanosensitive (HTM) afferents in the spinal dorsal horn, the majority of which contact more than 4 and up to 13 postsynaptic dendrites (Alvarez et al, 1992). A significant fraction of TRPV1+ terminals also participated in complex synaptic arrangements with three or more postsynaptic dendrites, analogous to the patterns of termination of the nonpeptidergic C fibers (Coimbra et al, 1974) and of glomerular terminals (Gobel, 1974; Gobel et al, 1981).…”

Ultrastructure and synaptology of the paratrigeminal nucleus in the rat: Primary pharyngeal and laryngeal afferent projections

“…Thus, there appear to be no striking differences in synaptic organization between trigeminal somatic and visceral afferents in the PTN. Further, the synaptic arrangements in the PTN are more like those of laminae I and II of SpVc, while in other trigeminal nuclei, e.g., the principal sensory nucleus and dorsomedial part of SpVi, complex synaptic arrangements (triads) involving primary afferents are more common (Bae et al, 2003(Bae et al, , 2004b(Bae et al, , 2005.…”

Synaptic connectivity of urinary bladder afferents in the rat superficial dorsal horn and spinal parasympathetic nucleus

“…The synaptic connectivities of the trigeminal low‐threshold mechanoreceptive (Aβ) afferent terminals are also different between the trigeminal main sensory nucleus and oral nucleus, which are primarily involved in processing the discriminative aspect of sensory information and actuating the jaw reflex, respectively (Bae et al, ). In contrast to the multiple studies on the synaptic connectivity of the various types of somatosensory afferents (Bae et al, , , ; Semba et al, ; Yeo et al, ), little has been done to decipher the synaptic connectivity of the visceral sensory afferents, which are anatomically and functionally distinct from their somatic analogues (for review, see Robinson & Gebhart, ; Sugiura, Terui, & Hosoya, ).…”