Synaptic organization of monosynaptic connections from mesencephalic trigeminal nucleus neurons to hypoglossal motoneurons in the rat

Synaptological characteristics of synapses between axonal boutons of the trigeminal mesencephalic nucleus (Vme) neurons and the hypoglossal nucleus (XII) motoneurons (MNs) were studied using biotinylated dextran amine (BDA) anterograde labeling combined with horseradish peroxidase (HRP) retrograde transport in the rat. BDA was initially iontophoresed into Vme unilaterally and 7 days later HRP was injected into the anterior two‐thirds of the ipsilateral tongue. After histochemical reactions, BDA anterogradely labeled boutons were seen to appose closely to somata and dendrites of HRP retrogradely labeled MNs in XII by light microscopy. A total of 212 BDA‐labeled Vme boutons were examined ultrastructurally, which had an average diameter of 1.3 ± 0.4 μm and contain small clear spherical vesicles. Eighty‐eight percent of Vme boutons (187/212) synapsed on dendrites of HRP‐labeled XII MNs. Twenty‐five Vme boutons (25/212, 12%) made synapses with somata of HRP‐labeled XII MNs. Thirty‐five percent (74/212) of BDA‐labeled Vme boutons were also contacted by unlabeled P‐type terminals. Presynaptic P‐type terminals contained spherical (47%, 35/74), pleomorphic (43%, 32/74), and flattened (10%, 7/74) synaptic vesicles. Thus, P‐type terminals (as a presynaptic element), BDA‐labeled Vme boutons, and XII MNs constitute axoaxodendritic and axoaxosomatic synaptic triads. There are four types of synaptic microcircuits in XII neuropil: synaptic convergence, synaptic divergence, presynaptic inhibition synaptic circuits, and feedforward regulation circuits. This detailed ultrastructure examination of the synaptic organization between Vme neurons and XII MNs provides insights into the synaptic mechanisms of the trigeminal proprioceptive afferents involved in the jaw–tongue reflex and coordination during oral motor behaviors. Synapse 49:157–169, 2003. © 2003 Wiley‐Liss, Inc.