Morphology and synaptic connections of slowly adapting periodontal afferent terminals in the trigeminal subnuclei principalis and oralis of the cat

Abstract

Previous studies suggest that sensory information from primary afferent fibers is processed in a distinct manner in the individual subnuclei of trigeminal sensory nuclear complex. The present study has addressed this issue by using intra-axonal labeling with horseradish peroxidase to examine the ultrastructure and synaptic organization of axon terminals from slowly adapting (SA) periodontal afferents in the ventral subdivision (Vpv) of principalis and the rostro-dorsomedial part (Vo.r) of oralis. Our observations are based on complete or near-complete reconstructions of 139 synaptic boutons in Vpv and 105 in Vo.r. All the labeled boutons contained clear, spherical, synaptic vesicles and were presynaptic to unlabeled dendrites, and they were frequently postsynaptic to unlabeled axon terminals containing pleomorphic synaptic vesicles (P-endings). The P-endings frequently formed axodendritic synapses on dendrites which received axodendritic synapses from labeled boutons (synaptic triads). On the basis of the number of contacts, synaptic arrangements associated with the labeled boutons could be subgrouped into simple (one or two contacts), intermediate (three or four contacts), and complex (five or more contacts) types. The labeled boutons varied from round to elongated forms with smooth to more irregular or scalloped contours. The boutons with scalloped contour were much more frequent in the complex type. The boutons of the intermediate type were significantly smaller than the complex type and larger than the simple type. The SA periodontal afferent terminals participated in each type of synaptic arrangements in Vpv, but were mostly of the simple type in Vo.r. The size of labeled boutons was significantly larger in Vpv than in Vo.r. The total number of axodendritic and axoaxonic contacts per labeled bouton was significantly higher in Vpv than in Vo.r. Another difference was the more frequent occurrence of synaptic triads in Vpv than in Vo.r. These observations provide evidence that sensory information from primary afferent fibers is processed in a different manner in the two subnuclei.

Ultrastructural observations of synaptic connections of vibrissa afferent terminals in cat principal sensory nucleus and morphometry of related synaptic elements

“…Vibrissa afferent boutons differed between SA and FA types in the frequency distribution of the three types of synaptic arrangement, especially in the existence of axosomatic contacts in SA afferents. When the present data are compared with those previously made on SA periodontal afferent boutons in Vp, a major difference noted is that the frequency of occurrence of axoaxonic contacts per bouton is higher in periodontal afferent boutons (2.03 Ϯ 0.49, see Table 2 in Bae et al, 1994) than that in vibrissa afferent boutons (SA, 0.95 Ϯ 1.19; FA, 1.22 Ϯ 1.15; Table 2): the frequency of axodendritic contacts per bouton is almost the same between the two fiber classes. The frequency of axoaxonic contacts per bouton of SA vibrissa afferents in Vp is almost the same as that of SA periodontal afferents in Vo and Vsup (Bae et al, 1996), but that of axodendritic contacts per bouton is higher in vibrissa afferents in Vp than in SA periodontal afferents in Vo and Vsup.…”

“…The size relation between primary afferent boutons and their postsynaptic dendrites appears to be less obvious in motoneurons, compared with sensorineuron synapses. The difference between motoneuron and sensorineuron synapses may be due to the existence of glomerular synapses that are frequently found between second-order sensorineurons and primary afferent terminals (Ralston, 1965(Ralston, , 1968(Ralston, , 1979Kerr, 1966Kerr, , 1970Kerr, , 1975Gobel, 1974Gobel, , 1976Gobel, , 1980Réthelyi et al, 1982;Semba et al, 1983Semba et al, , 1984Semba et al, , 1985Ralston et al, 1984;Bae et al, 1994; present study) but is only occasionally seen in synapses made by muscle spindle afferent terminals on motoneurons (Conradi et al, 1983;Fyffe and Light, 1984;Pierce and Mendell, 1993;Bae et al, 1996). The glomerular terminals have scalloped contours that are large and are surrounded by thin dendrites and P-endings and are most frequent in labeled boutons that participate in the complex synaptic arrangement ; present study).…”

“…We have searched unsuccessfully for vesicle-containing dendrites presynaptic to labeled boutons in the present study as well as in the previous studies (Sugimoto et al, 1991(Sugimoto et al, , 1992Bae et al, 1993Bae et al, , 1994Bae et al, , 1996. Dendroaxonic synapses, there- Figure 6 fore, cannot be deemed to be characteristic of the synaptic arrangements associated with low-and high-threshold mechanoreceptive fibers and with muscle spindle afferents in the trigeminal system.…”

“…The SA and FA boutons made axodendritic synapses, and they were frequently postsynaptic to P-endings. A paucity of axosomatic synapses is a feature common to sensory primary afferent terminals (Egger et al, 1981;Maxwell et al, 1982Maxwell et al, , 1984Réthelyi et al, 1982;Semba et al, 1983Semba et al, , 1984Semba et al, , 1985Ralston et al, 1984;Renehan et al, 1988;Sugimoto et al, 1991Sugimoto et al, , 1992Bae et al, 1994) but note that three SA vibrissa afferent boutons made axosomatic synapses. By contrast, a small but significant number of muscle spindle afferent terminals contact motoneuronal somata (Brown and Fyffe, 1981;Conradi et al, 1983;Pierce and Mendell, 1993;Bae et al, 1996).…”

“…Axon terminals presynaptic to labeled boutons from SA and FA vibrissa afferents may be GABAergic in origin. The presence of axoaxonic synapses is a feature common to a variety of functionally identified primary afferent terminals in the trigeminal sensory (Sugimoto et al, 1991(Sugimoto et al, , 1992Bae et al, 1993Bae et al, , 1994 and motor nuclei (Luo and Li, 1991;Luo et al, 1995;Bae et al, 1996) and in the spinal cord (Egger et al, 1981;Maxwell et al, 1982;Réthelyi et al, 1982;Conradi et al, 1983;Maxwell and Bannatyne, 1983;Semba et al, 1983Semba et al, , 1984Semba et al, , 1985Fyffe and Light, 1984;Ralston et al, 1984;Pierce and Mendell, 1993).…”