Corticofugal projections to trigeminal motoneurons innervating antagonistic jaw muscles in rats as demonstrated by anterograde and retrograde tract tracing

Abstract

Little is known about the organization of corticofugal projections controlling antagonistic jaw muscles. To address this issue, we employed retrograde (Fluorogold; FG) and anterograde (biotinylated dextran amine; BDA) tracing techniques in rats. Three groups of premotoneurons were identified by injecting FG into the jaw-closing (JC) and -opening (JO) subdivisions of the trigeminal motor nucleus (Vmo). These were 1) the intertrigeminal region (Vint) and principal trigeminal sensory nucleus for JC nucleus; 2) the reticular region medial to JO nucleus (RmJO) for JO nucleus; and 3) the parabrachial (Pb) and supratrigeminal (Vsup) nuclei, reticular regions medial and ventral to JC nucleus, rostrodorsomedial oralis (Vor), and juxtatrigeminal region (Vjuxt) containing a mixture of premotoneurons to both the nuclei. Subsequently, FG was injected into the representative premotoneuron structures. The JC and JO premotoneurons received main afferents from the lateral and medial agranular fields of motor cortex (Agl and Agm), respectively, whereas afferents to the nuclei with both JC and JO premotoneurons arose from Agl also and from primary somatosensory cortex (S1). Finally, BDA was injected into each of the three cortical areas representing the premotoneuron structures to complement the FG data. The Agl and Agm projected to reticular regions around the Vmo, whereas the Pb, Vsup, Vor, and Vjuxt received input from Agl. The S1 projected to the trigeminal sensory nuclei as well as to the Pb, Vsup, and Vjuxt. These results suggest that corticofugal projections to Vmo via premotoneuron structures consist of multiple pathways, which influence distinct patterns of jaw movements.

Oromotor Nuclei

“…Although one brief report describes a few direct cortico-trigeminal fibers, and short latency responses, that might result from descending cortical projections onto 5N dendrites that extend into the lateral tegmental field (Ohta and Sasamoto, 1980), the predominant view is that most forebrain pathways are not direct to 5N neurons, with the one likely exception of a projection from the hypothalamus. Thus, retrograde tracers injected into 5N label motor cortex, the central nucleus of the amygdala, the lateral hypothalamus and the bed nucleus of the stria terminalis, but complimentary anterograde marker injections into these forebrain sites typically result in considerably more label in the area surrounding 5N rather than within the nuclear boundaries, suggesting that retrograde injections spilled over into the adjacent RF (Mascaro et al, 2009;Yoshida et al, 2009). These descending projections to the RF however, show a degree of specificity (Fig.…”

“…The RF surrounding 5N projects bilaterally to 5N and includes cells in the supratrigeminal nucleus (Su5) located dorsal to 5N, the intertrigeminal nucleus (I5) interposed between 5N and the principal trigeminal sensory nucleus, and the juxtatrigeminal area (Jx5) ventral to 5N (Travers and Norgren, 1983;Vornov and Sutin, 1983;Rokx et al, 1986;Appenteng et al, 1990;Yoshida et al, 2009). More recently, the region just medial to the ventromedial subdivision of 5N (MPe5) has been identified as having a close association with adjacent jaw-opener motoneurons (McDavid et al, 2006;Yoshida et al, 2009).…”

“…2). The lateral region of the agranular motor cortex projects to the intertrigeminal region (I5) immediately adjacent to jaw-closing motoneurons in the dorsolateral 5N, and the more medial region of the agranular cortex projects to the medial peritrigeminal region (MPe5), medial to the ventromedial subdivision of 5N containing jaw-opening motoneurons (Yoshida et al, 2009). FIGURE 2 Some of the projections to the motor trigeminal nucleus are to specific subdivisions.…”

“…The RF surrounding 5N projects bilaterally to 5N and includes cells in the supratrigeminal nucleus (Su5) located dorsal to 5N, the intertrigeminal nucleus (I5) interposed between 5N and the principal trigeminal sensory nucleus, and the juxtatrigeminal area (Jx5) ventral to 5N (Travers and Norgren, 1983;Vornov and Sutin, 1983;Rokx et al, 1986;Appenteng et al, 1990;Yoshida et al, 2009). More recently, the region just medial to the ventromedial subdivision of 5N (MPe5) has been identified as having a close association with adjacent jaw-opener motoneurons (McDavid et al, 2006;Yoshida et al, 2009). These RF regions surrounding 5N (initially designated Regio h in rabbit (Meesen and Olszewski, 1949)) receive numerous inputs to influence 5N neurons, including projections from the red nucleus (Godefroy et al, 1998) the midline pontine and medullary RF (rabbit: Kolta et al, 2000), the central nucleus of the amygdala, lateral hypothalamus, the bed nucleus of the stria terminalis (Mascaro et al, 2009), and cortex (Yoshida et al, 2009).…”

Central Neural Mechanisms Involved in the Control of Jaw Movement during Postnatal Development

“…Such premotor neurons are distributed in various brain regions including the lateral reticular formation of the lower brainstem in the pons and medulla oblongata [6][7][8][9][10][11][12][13][14][15][16][17][18] . In addition, these premotor neurons also receive ascending and descending inputs from a number of regions : the orofacial structures [6][7][8] , the masticatory CPG 4,9 , the cerebral cortex 10,11 , the hypothalamus 12 , and the amygdala 13 . This neural architecture indicates that the neural circuits including premotor neurons and motoneurons are involved in controlling masticatory muscle activities via ascending and descending inputs during jaw movement.…”