“…When premotor neurons were labeled from viral injection into the left masseter muscle, we found that the right MoV nucleus was covered by fluorescently labeled axons (Video 1), indicating that many premotor neurons project to motor nuclei on both sides. This is consistent with previous dye tracing studies (Kamogawa et al, 1994; Yoshida et al, 2005; Kondo et al, 2006). However, because MoV contains both motoneurons and interneurons (Appenteng and Girdlestone, 1987; Ter Horst et al, 1990; Juch et al, 1993; McDavid et al, 2006), it is possible that these bilaterally projecting premotor neurons synapse with motoneurons on the ipsilateral side, and with interneurons on the contralateral side.…”
Section: Resultssupporting
confidence: 94%
“…We also observed labeled interneurons in the contralateral MoV in our tracing, however this labeling was very sparse (see Figure 3E,F, arrow heads). Additionally, previous studies using retrograde dyes have labeled some reticular neurons projecting to both the left and right MoV, suggesting that bilateral coordination may also arise from inputs other than MoV interneurons (Kamogawa et al, 1994; Yoshida et al, 2005). Our finding that masseter motoneurons on one side receive extensive premotor inputs from both ipsi- and contralateral reticular (Rt) neurons (Figure 2A–B) suggests that premotor neurons in the reticular formation may be involved in producing synchronized and symmetric jaw motor activity on both sides.10.7554/eLife.02511.009Figure 3.Evidence for the presence of bilateral-projecting masseter premotor neurons.( A – F ) Simultaneous tracing of left (ΔG-RV-EGFP, green) and right (ΔG-RV-mCherry, red) masseter premotor neurons.…”
Section: Resultsmentioning
confidence: 98%
“…By analogy, it is conceivable that different orofacial muscles are also controlled by different CPGs with their interaction resulting in orofacial coordination, although the evidence for well-defined jaw, face, and tongue CPGs is lacking. On the other hand, previous studies injecting two different retrograde tracers into two different cranial motor nuclei have suggested the existence of neurons projecting to both nuclei (Amri et al, 1990; Li et al, 1993; Kamogawa et al, 1994; Popratiloff et al, 2001; Kondo et al, 2006). However, due to limitations of the neural tracer technique, such as non-specific labeling of passing fibers and labeling of the entire nucleus rather than the motoneurons innervating specific muscles, whether there are common premotor neurons simultaneously innervating specific motoneuron groups enabling the above mentioned orofacial coordination remained unclear.…”
Feeding behaviors require intricately coordinated activation among the muscles of the jaw, tongue, and face, but the neural anatomical substrates underlying such coordination remain unclear. In this study, we investigate whether the premotor circuitry of jaw and tongue motoneurons contain elements for coordination. Using a modified monosynaptic rabies virus-based transsynaptic tracing strategy, we systematically mapped premotor neurons for the jaw-closing masseter muscle and the tongue-protruding genioglossus muscle. The maps revealed that the two groups of premotor neurons are distributed in regions implicated in rhythmogenesis, descending motor control, and sensory feedback. Importantly, we discovered several premotor connection configurations that are ideally suited for coordinating bilaterally symmetric jaw movements, and for enabling co-activation of specific jaw, tongue, and facial muscles. Our findings suggest that shared premotor neurons that form specific multi-target connections with selected motoneurons are a simple and general solution to the problem of orofacial coordination.DOI:
http://dx.doi.org/10.7554/eLife.02511.001
“…When premotor neurons were labeled from viral injection into the left masseter muscle, we found that the right MoV nucleus was covered by fluorescently labeled axons (Video 1), indicating that many premotor neurons project to motor nuclei on both sides. This is consistent with previous dye tracing studies (Kamogawa et al, 1994; Yoshida et al, 2005; Kondo et al, 2006). However, because MoV contains both motoneurons and interneurons (Appenteng and Girdlestone, 1987; Ter Horst et al, 1990; Juch et al, 1993; McDavid et al, 2006), it is possible that these bilaterally projecting premotor neurons synapse with motoneurons on the ipsilateral side, and with interneurons on the contralateral side.…”
Section: Resultssupporting
confidence: 94%
“…We also observed labeled interneurons in the contralateral MoV in our tracing, however this labeling was very sparse (see Figure 3E,F, arrow heads). Additionally, previous studies using retrograde dyes have labeled some reticular neurons projecting to both the left and right MoV, suggesting that bilateral coordination may also arise from inputs other than MoV interneurons (Kamogawa et al, 1994; Yoshida et al, 2005). Our finding that masseter motoneurons on one side receive extensive premotor inputs from both ipsi- and contralateral reticular (Rt) neurons (Figure 2A–B) suggests that premotor neurons in the reticular formation may be involved in producing synchronized and symmetric jaw motor activity on both sides.10.7554/eLife.02511.009Figure 3.Evidence for the presence of bilateral-projecting masseter premotor neurons.( A – F ) Simultaneous tracing of left (ΔG-RV-EGFP, green) and right (ΔG-RV-mCherry, red) masseter premotor neurons.…”
Section: Resultsmentioning
confidence: 98%
“…By analogy, it is conceivable that different orofacial muscles are also controlled by different CPGs with their interaction resulting in orofacial coordination, although the evidence for well-defined jaw, face, and tongue CPGs is lacking. On the other hand, previous studies injecting two different retrograde tracers into two different cranial motor nuclei have suggested the existence of neurons projecting to both nuclei (Amri et al, 1990; Li et al, 1993; Kamogawa et al, 1994; Popratiloff et al, 2001; Kondo et al, 2006). However, due to limitations of the neural tracer technique, such as non-specific labeling of passing fibers and labeling of the entire nucleus rather than the motoneurons innervating specific muscles, whether there are common premotor neurons simultaneously innervating specific motoneuron groups enabling the above mentioned orofacial coordination remained unclear.…”
Feeding behaviors require intricately coordinated activation among the muscles of the jaw, tongue, and face, but the neural anatomical substrates underlying such coordination remain unclear. In this study, we investigate whether the premotor circuitry of jaw and tongue motoneurons contain elements for coordination. Using a modified monosynaptic rabies virus-based transsynaptic tracing strategy, we systematically mapped premotor neurons for the jaw-closing masseter muscle and the tongue-protruding genioglossus muscle. The maps revealed that the two groups of premotor neurons are distributed in regions implicated in rhythmogenesis, descending motor control, and sensory feedback. Importantly, we discovered several premotor connection configurations that are ideally suited for coordinating bilaterally symmetric jaw movements, and for enabling co-activation of specific jaw, tongue, and facial muscles. Our findings suggest that shared premotor neurons that form specific multi-target connections with selected motoneurons are a simple and general solution to the problem of orofacial coordination.DOI:
http://dx.doi.org/10.7554/eLife.02511.001
“…Amongst the afferents to TSC neurons, those arising from the VN and PH have been described in many previous studies (Lowick and Wolstencroft 1983;Walberg et al 1985;Marfurt and Rajchert 1991;Buisseret-Delmas 1999;Valla et al 2003). TSC premotor neurons have been suggested to integrate the rhythmic drive from the masticatory central pattern generator with descending cortical commands in order to optimize the temporal patterning and the relative amplitude of mandibular muscle activity (Kamogawa et al 1994;Inoue et al 2002). The present data raise the possibility that vestibular signals could modulate the processing of signals by TSC neurons to account for the animal's head position and/or head movements.…”
Previous studies reported that the activity of trigeminal motoneurons innervating masseter muscles is modulated by vestibular inputs. We performed the present study to provide an anatomical substrate for these physiological observations. The transynaptic retrograde tracer pseudorabies virus-Bartha (PRV-BA) was injected into multiple sites of the lower third of the superficial layer of the masseter muscle in rats, a subset of which underwent a sympathectomy prior to virus injections, and the animals were euthanized 24-120 hrs later. Labeled masseteric motoneurons were first found in the ipsilateral trigeminal motor nucleus following a 24-hr post inoculation period; subsequent to 72-hr survival times, the number of infected motoneurons increased, and at ≥ 96-hrs many of these cells showed signs of cytopathic changes. Following 72-hr survival times, a few transynaptically-labeled neurons appeared bilaterally in the medial vestibular nucleus (MVe) and the caudal prepositus hypoglossi (PH) and in the ipsilateral spinal vestibular nucleus (SpVe). At survival times of 96-120 hrs, labeled neurons were consistently observed bilaterally in all vestibular nuclei (VN), although the highest concentration of infected cells was located in the caudal part of the MVe, the SpVe, and the caudal portion of PH. The distribution and density of labeling in the VN and PH were similar in sympathectomized and non-sympathectomized rats. These anatomical data provide the first direct evidence that neurons in the VN and PH project bilaterally to populations of motoneurons innervating the lower third of the superficial layer of the masseter muscle. The MVe, PH, and SpVe appear to play a predominant integrative role in producing vestibulo-trigeminal responses.
“…The supratrigeminal region is a cluster of neurons that border the dorsal cap of the TMN (reviewed in Kamogawa et al, 1994) and, according to immunohistochemical and electrophysiological studies, contains excitatory and inhibitory interneurons, many of which project to the TMN (Goldberg and Nakamura, 1968;Turman and Chandler, 1994a,b;Li et al, 2005; among others). Historically, this region has received much attention for its role in producing glycinergic inhibition of jaw-closer motoneurons during jaw-opening reflexes (Goldberg and Nakamura, 1968;Kidokoro et al, 1968).…”
The membrane properties and morphological features of interneurons in the supratrigeminal area (SupV) were studied in rat brain slices using whole-cell patch clamp recording techniques. We classified three morphological types of neurons as fusiform, pyramidal, and multipolar and four physiological types of neurons according to their discharge pattern in response to a 1-sec depolarizing current pulse from -80 mV. Single-spike neurons responded with a single spike, phasic neurons showed an initial burst of spikes and were silent during the remainder of the stimulus, delayed-firing (DF) neurons exhibited a slow depolarization and delay to initial spike onset, and tonic (T) neurons showed maintained a discharge throughout the stimulus pulse. In a subpopulation of neurons (10%), membrane depolarization to around -44 mV produced a rhythmic burst discharge (RB) that was associated with voltage-dependent subthreshold membrane oscillations. Both these phenomena were blocked by the sodium channel blocker riluzole at a concentration that did not affect the fast transient spike. Low doses of 4-AP, which blocks low-threshold K+ currents, transformed bursting into low-frequency tonic discharge. In contrast, bursting occurred with exposure to cadium, a calcium-channel blocker. This suggests that persistent sodium currents and low-threshold K+ currents have a role in intrinsic burst generation. Importantly, RB cells were most often associated with multipolar neurons that exhibited either a DF or a T discharge. Thus, the SupV contains a variety of physiological cell types with unique morphologies and discharge characteristics. Intrinsic bursting neurons form a unique group in this region. .
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