Neuronal circuitry and synaptic organization of trigeminal proprioceptive afferents mediating tongue movement and jaw–tongue coordination via hypoglossal premotor neurons

Abstract

The neural framework and synaptic organization of trigeminal proprioceptive afferent-mediated jaw-tongue coordination were studied in rats using multiple electrophysiological and neuroanatomical approaches. Electrostimulation of the masseter nerve evoked short-latency responses (5.86 +/- 2.59 ms) in hypoglossal premotor pools including the parvocellular (PCRt) and intermediate (IRt) reticular nuclei and the dorsomedial part of the spinal trigeminal nucleus oralis (Vodm) and interpolaris (Vidm). Biocytin-labelled axon terminals from these areas traveled into the hypoglossal nucleus (XII) and contacted motoneurons. Double labelling of biotinylated dextran amine (BDA) tracing and cholera toxin B (CTB) transport demonstrated that labelled axons and terminals from the mesencephalic trigeminal nucleus (Vme) overlapped with XII premotor neurons in the alpha division and in PCRt, IRt, Vodm and Vidm. Confocal microscopic observations revealed that Vme terminals closely contacted XII premotor neurons. Dual labelling of intracellular neurobiotin staining of jaw-muscle spindle afferents (JMSAs) combined with horseradish peroxidase (HRP) retrograde transport revealed that 498 JMSA boutons apposed to 146 HRP-labelled premotor neurons. Electron microscopic observations demonstrated that 127 JMSA boutons made both axodendritic (68%) and axosomatic (32%) synapses with XII premotor neurons. Eighty-three per cent of synapses were asymmetric and the rest (17%) were symmetric. Thirty-nine per cent of JMSA boutons received presynaptic contacts from P-type terminals. Varieties of synaptic organizations were found. These results provide evidence that trigeminal proprioceptive afferents mediate jaw-tongue coordination through XII premotor neurons. Ultrastructural findings demonstrated that synapses between JMSA boutons and XII premotor neurons are predominantly excitatory, and synaptic transmission to XII motoneurons is modified on XII premotor neurons by presynaptic mechanisms. These frameworks and synaptic organizations are most probably the neural substrate for trigeminal proprioceptive afferent-mediated jaw-tongue coordination.

Central nervous system distribution of the transcription factor Phox2b in the adult rat

“…The present results suggest that Phox2b might also govern the development of trigeminal premotor cells. Although the hypoglossal nucleus does not depend on Phox2b for development and did not contain this protein in the adult, Phox2b was heavily present in regions known to contain hypoglossal premotor neurons (Luo et al, 2006), namely, the dorsal aspects of the parvocellular reticular formation (PCRt) and intermediate reticular nucleus (IRt) and, most particularly, the dorsomedial spinal trigeminal nucleus (DMsp5; nomenclature after Paxinos and Watson, 1998). Developmental problems associated with the motor innervation of the orofacial sphere are consistent with the feeding problems commonly experienced by infants with CCHS and may be related to the distinctive facial features present in patients with confirmed Phox2b-dependent CCHS (Todd et al, 2006).…”

A novel slice preparation to study medullary oromotor and autonomic circuits in vitro

“…Pre-oromotor neurons of the hypoglossal and trigeminal motor nuclei are located in a column that extends from the pontomedullary junction into the pons (Travers et al, 2005; Luo et al, 2006). Projections from this region are found throughout most of the hindbrain both ipsi- and contra-laterally.…”

“…Many pre-oromotor neurons innervating the tongue and jaw are located in the medullary reticular formation subjacent to the NST (Travers and Rinaman, 2002; Luo et al, 2006). These pre-oromotor neurons extend ventral and at a slight angle off the midline to a depth of up to 1.5 mm from the ventral border the NST (Travers et al, 2005).…”

Oromotor Nuclei

“…Although some controversy exists as to whether Me5 projects directly to 12N via Probst's tract (see : Lowe, 1981;Zhang et al, 2001) or onto dendrites of 12N motoneurons extending laterally into the adjacent RF (Matesz, 1981;Ruggiero et al, 1982), work combining anterograde, retrograde and electron microscopy have clearly demonstrated a Me5 12N projection . Proprioceptive information from jaw muscles may also reach 12N indirectly through the Su5 as well as neurons in the PCRt and IRt (Mizuno and Sauerland, 1970;Matesz, 1981;Luo et al, 2006).…”