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

Abstract

Previous work suggests that slowly adapting (SA) periodontal afferents have different synaptic arrangements in the principal (Vp) and oral trigeminal nuclei and that the synaptic structure associated with transmitter release may be related directly to bouton size. The present study examined the ultrastructures of SA and fast adapting (FA) vibrissa afferents and their associated unlabeled axonal endings in the cat Vp by using intra-axonal labeling with horseradish peroxidase and a morphometric analysis. All SA and FA afferent boutons contained clear, round, synaptic vesicles. All the FA and most SA boutons were presynaptic to dendrites, but a few SA boutons were axosomatic. Both types of bouton were frequently postsynaptic to unlabeled axonal ending(s) containing pleomorphic, synaptic vesicles (P-ending). The size of labeled boutons was larger in FA than SA afferents, but the size of dendrites postsynaptic to labeled boutons was larger for SA than FA afferents. Large-sized FA and SA boutons made synaptic contacts with small-diameter dendrites. The size of FA and SA boutons was larger than that of their associated P-endings. A morphometric analysis made on the pooled data of SA and FA boutons indicated that apposed surface area, active zone number, total active zone area, vesicle number, and mitochondrial volume were highly correlated in a positive linear manner with labeled bouton volume. These relationships were also applicable to unlabeled P-endings, but the range of each parameter was smaller than that of the labeled boutons. These observations provide evidence that the two functionally distinct types of vibrissa afferent manifest unique differences but share certain structural features in the synaptic organization and that the ultrastructural "size principle" proposed by Pierce and Mendell ([1993] J. Neurosci. 13:4748-4763) for Ia-motoneuron synapses is applicable to the somatosensory system.

Ultrastructural analysis of low-threshold mechanoreceptive vibrissa afferent boutons in the cat trigeminal caudal nucleus

“…These characteristics suggest that bouton size is directly associated with its capacity for synaptic release and may underlie potential synaptic efficacy or strength of the boutons (Pierce & Lewin, 1994). This is consistent with the findings of the tooth pulp afferents in the TSN (Bae et al, 2004), vibrissa afferents in the Vp (Nakagawa et al, 1997) and Vi (Moon et al, 2008), and slowly adapting lingual afferents in the Vp and Vo (Zhang et al, 2001). These findings also suggest that the "size principle" proposed by the Pierce & Mendell (1993) in the Ia-motoneuron synapse is also applicable to the trigeminal sensory afferents in the 1st relay nuclei of the brain stem.…”

“…These findings signify that the strength of presynaptic modulation for the activity of vibrissa afferent boutons depends on the number of p-endings in the Vc. It is also observed in the vibrissa afferent boutons in Vi and Vp (Nakagawa et al, 1997; Moon et al, 2008), pulpal afferents in TSN (Bae et al, 2004) and Ia spindle afferents in the spinal ventral horn (Pierce & Mendell, 1993). It provides a notion that presynaptic modulation depending on the number of p-endings may be a general rule controlling the synaptic release of the primary afferent boutons.…”

“…In addition, we also showed that, in the Vi, the vibrissa afferent receives extensive presynaptic modulation through axoaxonic synapse and large majority of p-endings presynaptic to the vibrissa afferent boutons contain both γ-aminobutyric acid (GABA) and glycine. The vibrissa afferent boutons were also quantitatively analyzed in the Vi and Vp (Nakagawa et al, 1997; Moon et al, 2008). Thus, bouton volume of the vibrissa afferents is much larger than the p-endings, and the bouton size is more widely distributed in the Vi than in the Vp.…”

Whisker-related circuitry in the trigeminal nucleus principalis: Ultrastructure

“…As such, complex permutations exist for modulation of PrV cell responsiveness to whisker deflection. Our results confirm and extend those of others (Nakagawa et al 1997;Bae et al 2000Bae et al , 2005Moon et al 2008) that have described GABA (and glycine) immunoreactivity in axonal endings presynaptic to whisker primary afferent terminals in PrV (and SpV subnucleus interpolaris) in the cat, which lacks barrels.…”

Identification of ?-aminobutyric acid-immunoreactive axon endings associated with mesencephalic periodontal afferent terminals and morphometry of the two types of terminals in the cat supratrigeminal nucleus

“…It has been reported that, as mentioned above, active zone number and size are associated with synaptic strength or the level of transmitter release (Bower and Haberly, 1986;Chiang and Govind, 1986;Desmond and Levy, 1986;Lnenicka et al, 1986;Propst and Ko, 1987;Bailey and Chen, 1989) and that these synaptic parameters are positively correlated with bouton volume (Yeow and Peterson, 1991;Pierce and Mendell, 1993;Nakagawa et al, 1997). The present results showing that bouton volume, active zone size, and mitochondrial volume were smaller in GABA-IR P-endings than labeled boutons suggest that GABA receptors mediating presynaptic inhibition can be activated with a smaller amount of transmitter (GABA) released, and the resultant local synaptic current is also smaller compared with receptors mediating postsynaptic excitation.…”