Identification of brainstem interneurons projecting to the trigeminal motor nucleus and adjacent structures in the rabbit
Introduction
The basic network responsible for generation of rhythmic jaw movements is located in the brain stem. The most recent evidence suggests that this network lies between the rostral poles of the trigeminal (N.V.mt) and facial (N.VII) motor nuclei, but the medio-lateral limits are not yet defined. Although Tanaka et al. (1999) have recently implied that the lateral reticular formation extending 200–400 μm medial to N.V.mt suffices to generate rhythmic motor activity, this evidence is not conclusive, because the activity was induced by a pharmacological mixture that produces rhythmical membrane potential fluctuations in motoneurons deprived of synaptic input (Kim and Chandler, 1995). Nevertheless, it is clear from other studies that the circuitry for generation of rhythmic jaw movements does include the lateral brainstem surrounding N.V.mt (Donga and Lund, 1991, Inoue et al., 1992, Westberg et al., 1998). This region contains Regio h (the reticular zone surrounding N.V.mt that is composed of the supratrigeminal area dorsally, the intertrigeminal area laterally and the juxtatrigeminal area medially), the rostral part of the V spinal nucleus (N.V.spo γ) and the parvocellular reticular formation adjacent to it (R.pc α). Neurons in all these regions project to N.V.mt of both sides (Mizuno et al., 1978, Mizuno et al., 1983, Travers and Norgren, 1983, Li et al., 1995) and change their firing frequency during mastication (Moriyama, 1987, Donga and Lund, 1991, Inoue et al., 1992, Westberg et al., 1995).
However, there are also neurons in the medial reticular formation that appear to participate in the genesis of mastication. In guinea pigs, neurons in and around the rostral pole of nucleus giganto-cellularis (Rgc) fire tonically during mastication induced by cortical stimulation, and a group of neurons lying dorsal to these are rhythmically active (Chandler and Tal, 1986, Nozaki et al., 1986a, Nozaki et al., 1986b, Chandler et al., 1990). In rabbits, similar groups of neurons have been described in the ventral and dorsal nucleus pontis caudalis (nPC) (Lund et al., 1998). We hypothesize that these medial groups act as a rhythm generator, while the lateral groups generate motoneuron bursts by integrating sensory information and descending commands with the masticatory rhythm generated medially (Lund et al., 1998). This is similar to some models that have been proposed for other complex rhythmic behaviours in mammals (e.g. respiration, Feldman et al., 1988).
In an attempt to provide anatomical support for this model, we have compared populations of neurons projecting to V motoneurons of rabbits to those projecting to a component of the putative burst generator, namely Regio h. To gain insight on how these areas are functionally linked we also attempted to identify subpopulations of excitatory and inhibitory neurons by combining the tract tracing technique with immunohistochemistry against glutamate and GABA.
Section snippets
Materials and methods
Six male New Zealand white rabbits were used for the experiments. The animals were anaesthetized with urethane (1 g kg−1, i.v.). The trachea was intubated and the femoral vein was cannulated for administration of drugs and for fluid replacement. The ECG was recorded. The masseter and inferior alveolar nerves were prepared for electrical stimulation as described previously (Olsson et al., 1986a). Wounds were closed, the animal was transferred to a stereotaxic frame, and an opening was made in
Results
One of the six injected animals was excluded from analysis because the retrograde and immunochemical labelling were very faint and suggested that there was a problem either during the survival period or the subsequent perfusion. The five remaining injection sites are shown in Fig. 1. In two cases (R1 and R3), small injections were made within the boundaries of N.V.mt, although some spread was seen dorsally along the electrode track in R1. In a third (R5), the core of a larger injection was also
Immunoreactivity of retrogradely labelled neurons
Fig. 6 shows two retrogradely labelled cells in nPC of R5 that were immunoreactive to glutamate and GABA antibodies (left and right panels respectively). Table 3 gives, for R1, 3, 4 and 5, the number of double labelled neurons for the nuclei containing most of the retrograde labelling (listed in Table 2). These numbers are also expressed as the percentage of total number of labelled cells in the structure identified in the first column. The bottom line (total) gives the total number of
Discussion
In the present study, we attempted to identify the anatomical pathway linking areas of the caudal pontine medial reticular formation (nPC) that play a role in mastication to trigeminal motoneurons using retrograde tracing techniques. We also tried to identify among these retrogradely labelled neurons those that were inhibitory and excitatory on the basis of their immunoreactivity to GABA and glutamate respectively. The results show that neurons of nPC have virtually no projections to N.V.mt,
Conclusion
The present study provides anatomical support for the hypothesis that the medial reticular formation has a role in the control of trigeminal motoneurons via direct projections from the caudal gigantocellular nucleus, and through a more important indirect connection from nucleus pontis caudalis via relays in Regio h. Regio h and the more caudal parts of the lateral parvocellular reticular formation are rich in last-order interneurons, many of which are also immunoreactive to GABA and glutamate.
Acknowledgements
The authors wish to sincerely thank Professor E.G. Jones and T. Hashikawa for their help with the immunohistochemical work, which was carried out at the RIKEN Institute, Wako, Japan. We are also grateful to Danielle Veilleux and Julie Martin for their technical assistance. This work was supported by a Group Grant from the Canadian MRC (#GR-176), the Canadian natural sciences and engineering research council (# OGP0172682) and the Swedish MRC (B93-04X- 00045-29A; K93-24P-10133-02A).
References (76)
- et al.
The nuclei of origin of brainstem enkephalin and cholecystokinin projections to the spinal trigeminal nucleus of the rat
Neuroscience
(1987) - et al.
The location of brainstem neurons which project bilaterally to the spinal trigeminal nuclei as demonstrated by the double fluorescent retrograde tracer technique
Brain Res.
(1983) - et al.
Solitarial premotor neuron projections to the rat esophagus and pharynx: implications for control of swallowing
Gastroenterology
(1998) - et al.
Cells of origin of the frontal projections to magnocellular and parvocellular red nucleus and superior colliculus in cynomolgus monkey. An HRP study
Neurosci. Lett.
(1979) Evidence for excitatory amino acid transmission between mesencephalic nucleus of V afferents and jaw-closer motoneurons in the guinea pig
Brain Res.
(1989)- et al.
The effects of nanoliter ejections of Lidocaine into the pontomedullary reticular formation on cortically induced rhythmical jaw movements in the guinea pig
Brain Res.
(1990) - et al.
Identification of rat brainstem multisynaptic connections to the oral motor nuclei using pseudorabies virus I. Masticatory muscle motor systems
Brain Res. Rev.
(1997) - et al.
Identification of rat brainstem multisynaptic connections to the oral motor nuclei in the rat using pseudorabies virus II. Facial muscle motor systems
Brain Res. Rev.
(1997) - et al.
Identification of rat brainstem multisynaptic connections to the oral motor nuclei using pseudorabies virus III. Lingual muscle motor systems
Brain Res. Rev.
(1997) - et al.
Glutamate as a CNS transmitter. I. Evaluation of glucose and glutamine as precursors for the synthesis of preferentially released glutamate
Brain Res.
(1979)
An anatomical study of brainstem projections to the trigeminal motor nucleus of lampreys
Neuroscience
Efferent projections of the parvocellular reticular nucleus to the mesencephalic trigeminal nucleus in rat
Brain Res.
Brainstem mechanisms underlying feeding behaviors
Curr. Opin. Neurobiol.
Commissural interneurons for masticatory motoneurons: A light and electron microscope study using the horseradish peroxidase tracer technique
Exp. Neurol.
Rhythmical jaw movements and lateral ponto-medullary reticular neurons in rats
Comp. Biochem. Physiol. [A]
Quantitative analysis and postsynaptic targets of GABA-immunoreactive boutons within the rat trigeminal motor nucleus
Brain Res.
Afferent connections of the nuclei reticularis pontis oralis and caudalis: a horseradish peroxidase study in the rat
Neuroscience
Distribution of serotonin-immunoreactivity in the central nervous system of the rat-cell bodies and terminals
Neuroscience
Localization of oral-motor rhythmogenic circuits in the isolated rat brainstem preparation
Brain Res.
Immunohistochemical localization of glutamate and glutaminase in guinea pig trigeminal premotoneurons
Brain Res.
An autoradiographic analysis of ascending projections from the medullary reticular formation in the rat
Neuroscience
Glycine-immunoreactive terminals in the rat trigeminal motor nucleus: light-and electron-microscopic analysis of their relationships with motoneurons and with GABA-immunoreactive terminals
Brain Res.
Nigral axon terminals are in contact with parvicellular reticular neurons which project to the motor trigeminal nucleus in the rat
Brain Res.
Central integration of swallow and airway-protective reflexes
Am. J. Med.
Brainstem viscerotopic organization of afferents and efferents involved in the control of swallowing
Am. J. Med.
Organisation of reciprocal connections between trigeminal and vestibular nuclei in the rat
J. Comp Neurol.
Neuroanatomy of the oculomotor system. The reticular formation
Rev. Oculomot. Res.
The effects of brain stem transections on the neuronal networks responsible for rhythmical jaw muscle activity in the guinea pig
J. Neurosci.
Cellular basis of pontine ponto-geniculo-occipital wave generation and modulation
Cell Mol. Neurobiol.
Trigeminal integration of vestibular and forelimb nerve inputs
Arch. Ital. Biol.
Differential innervation of protruder and retractor muscles of the tongue in the rat
J. Comp. Neurol.
Discharge patterns of trigeminal commissural last-order interneurons during fictive mastication in the rabbit
J. Neurophysiol.
Afferents to the nucleus reticularis parvicellularis of the cat medulla oblongata: a tract-tracing study with cholera toxin B subunit
J. Comp. Neurol.
Nuclei of origin of monoaminergic, peptidergic, and cholinergic afferents to the cat trigeminal motor nucleus: A double-labeling study with cholera-toxin as a retrograde tracer
J. Comp. Neurol.
GABAA-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits
J. Comp. Neurol.
Intracellular analysis of trigeminal motoneuron rhythmical activity during stimulation of pontomedullary reticular formation in anesthetized guinea pig
J. Neurophysiol.
The perihypoglossal projection to the superior colliculus in the rhesus monkey
Vis. Neurosci
Cited by (82)
Revisiting the supratrigeminal nucleus in the rat
2016, Neuroscience