Differential distribution of cell bodies and central axons of mesencephalic trigeminal nucleus neurons supplying the jaw-closing muscles and periodontal tissue: A transganglionic tracer study in the cat

doi:10.1016/0006-8993(85)91442-8

Brain Research

Volume 359, Issues 1–2, 16 December 1985, Pages 311-319

https://doi.org/10.1016/0006-8993(85)91442-8 Get rights and content

Distribution of cell bodies and central axons of mesencephalic trigeminal nucleus (MTN) neurons were examined in the cat by the method of transganglionic transport of horseradish peroxidase (HRP). Jaw-closing muscle afferent MTN neurons were distributed throughout the whole rostrocaudal extent of the MTN, and sent their axons ipsilaterally to the supratrigeminal and intertrigeminal regions, dorsolateral division of the motor trigeminal nucleus, lateral part of the medullary reticular formation, lamina VI of C1–C3 cord segments, and cerebellum. On the other hand, periodontal receptor afferent MTN neurons were located mainly in the caudal part of the MTN, and sent their axons ipsilaterally to the supratrigeminal region and cerebellum. The existence of multipolar MTN neurons with 1–9 smooth dendrites was also confirmed; most of them were jaw-closing muscle afferent neurons.

References (53)

AmanoN. et al.
Response characteristics of primary periodontal mechanoceptive neurons in the trigeminal mesencephalic nucleus to trapezoidal mechanical stimulation of a single tooth in the rat
Brain Research
(1982)
CapraN.F. et al.
Simultaneous demonstration of neuronal somata that innervate the tooth pulp and adjacent periodontal tissues, using two retrogradely transported anatomic markers
Exp. Neurol.
(1984)
Gonzálo-SanzL.M. et al.
Fibers of trigeminal mesencephalic neurons in the maxillary nerve of the rat
Neurosci. Lett.
(1980)
ManniE. et al.
Eye muscle proprioception and the semilunar ganglion
Exp. Neurol.
(1966)
ManniE. et al.
Peripheral pathway of eye muscle proprioception
Exp. Neurol.
(1968)
MateszC.
Peripheral and central distribution of fibres of the mesencephalic trigeminal root in the rat
Neurosci. Lett.
(1981)
MizunoN. et al.
Commissural interneurons for masticatory motoneurons: a light and electron microscope study using the horseradish peroxidase tracer technique
Exp. Neurol.
(1978)
NomuraS. et al.
Multipolar neurons and axodendritic synapses in the mesencephalic trigeminal nucleus of the cat
Neurosci. Lett.
(1985)
NomuraS. et al.
Central distribution of primary afferent fibers in the Arnold's nerve (the auricular branch of the vagus nerve): a transganglionic HRP study in the cat
Brain Research
(1984)
SmithR.D.
Location of the neurons innervating tendon spindles of masticator muscles
Exp. Neurol.
(1969)

StreitP. et al.

A new and sensitive staining method for axonally transported horseradish peroxidase (HRP) in the pigeon visual system

Brain Research

(1977)

WalbergF.

On the morphology of the mesencephalic trigeminal cells. New data based on tracer studies

Brain Research

(1984)

WanX.S.T. et al.

Cytoarchitecture of the extranuclear and commissural dendrites of hypoglossal nucleus neurons as revealed by conjugates of horseradish peroxidase with cholera toxin

Exp. Neurol.

(1982)

Alvarado-MallartR.M. et al.

Mesencephalic projections of the rectus lateralis muscle afferents in the cat

Arch. Ital. Biol.

(1975)

AppentengK. et al.

The projection of jaw elevator muscle spindle afferents to fifth nerve motoneurones in the cat

J. Physiol. (London)

(1978)

BrodalA. et al.

Retrograde cellular changes in the mesencephalic trigeminal nucleus in the cat following cerebellar lesions

Acta Morphol. Neerl.-Scand.

(1965)

CodyF.W.J. et al.

Distribution of tooth receptor afferents in the mesencephalic nucleus of the fifth cranial nerve

J. Physiol. (London)

(1974)

CodyF.W.J. et al.

A functional analysis of the components of the mesencephalic nucleus of the fifth nerve in the cat

J. Physiol. (London)

(1972)

CooperS. et al.

Nerve impulses in the brainstem of the goat: short latency responses obtained by stretching the extrinsic eye muscles and jaw muscles

J. Physiol. (London)

(1953)

CorbinK.B.

Observations on the peripheral distribution of fibres arising in the mesencephalic nucleus of the fifth cranial nerve

J. Comp. Neurol.

(1940)

CorbinK.B. et al.

Function of mesencephalic root of fifth cranial nerve

J. Neurophysiol.

(1940)

CupedoR.N.J.

A trigeminal midbrain-cerebellar fiber connection in the rat

J. Comp. Neurol.

(1965)

DaceyD.M.

Axon morphology of mesencephalic trigeminal neurons in a snake

Thamnophis sirtalis, J. Comp. Neurol.

(1982)

EbbesonS.O.E.

Projections of the optic tectum and the mesencephalic nucleus of the trigeminal nerve in the tegulizard (Upinabis nigropunctatus)

Cell Tissue Res.

(1981)

FillenzM.

Responses in the brainstem of the cat to stretch of extrinsic ocular muscles

J. Physiol. (London)

(1955)

GottliebS. et al.

The distribution of afferent neurones in the mesencephalic nucleus of the fifth nerve in the cat

J. Comp. Neurol.

(1984)

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Premotoneuronal inputs to early developing trigeminal motoneurons
2017, Journal of Oral Biosciences
Citation Excerpt :
The activities of the jaw-closing muscles are more easily facilitated by the physical properties of food compared to the activities of the jaw-opening muscles through the activation of periodontal and spindle afferents [2,3,21]. The SupV receives periodontal and spindle afferent inputs [22–25], and the premotor neurons that target the MoV and that are rhythmically active during the jaw-closing phase of cortically induced fictive mastication have been identified in the SupV of anesthetized and immobilized rats [9]. Thus, we identified that the pattern of inputs from the l-SupV and m-SupV to the MMNs was dominant compared to the inputs to the DMNs.
We previously reported that masseter motoneurons (MMNs) and digastric motoneurons (DMNs) in postnatal day (P) 1–5 rats receive convergent inputs from the lateral (l-) and medial (m-) supratrigeminal regions (SupV), intertrigeminal region (IntV), and dorsal region of the principal sensory trigeminal nucleus (PrV). The l-SupV sends burst inputs predominantly to the MMNs. We compared the synaptic inputs to P9–12 rat MMNs and DMNs with those found in the previous study involving P1–5 rats.
We performed whole-cell recordings and laser photolysis of caged glutamate in the MMNs and DMNs of P9–12 rats.
Similar to P1–5 rats, the photostimulation of multiple regions within the l-SupV, m-SupV, IntV, and dorsal PrV, induced postsynaptic currents (PSCs) in both P9–12 MMNs and DMNs. Photostimulation induced predominantly low-frequency PSCs in both P9–12 motoneurons, whereas l-SupV photostimulation predominantly induced burst PSCs in P1–5 rats. However, when the caged glutamate concentration was doubled, l-SupV photostimulation evoked burst PSCs in all P9–12 MMNs. Furthermore, l-SupV and m-SupV photostimulation evoked burst or low-frequency PSCs at significantly higher rates in the MMNs compared to in the DMNs.
These results suggested that, similar to P1–5 motoneurons, both P9–12 motoneurons received convergent inputs from the SupV, IntV, and PrV; however, the input–output gains of some of the premotor neurons decreased. These synaptic input changes may contribute to the proper development of chewing.
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Citation Excerpt :
The Vmes neurons receiving direct projection from the LHbl were distributed in entire rostrocaudal levels of Vmes, but the rostral Vmes neurons received stronger LHb projection than the caudal Vmes. It is well known that the somata of Vmes neurons innervating the masticatory muscle spindle are located rostrocaudally throughout the Vmes, whereas those innervating the periodontal ligaments are located only in its caudal half (Cody et al., 1972; Gonzálo-Sanz and Insausti, 1980; Jerge, 1963; Nomura and Mizuno, 1985). Therefore, the present results suggest that the spindle Vmes neurons in the rostral Vmes receive stronger inputs from the LHbl, and that the periodontal Vmes neurons receive weaker inputs.
Trigeminal mesencephalic nucleus (Vmes) neurons are primary afferents conveying deep sensation from the masticatory muscle spindles or the periodontal mechanoreceptors, and are crucial for controlling jaw movements. Their cell bodies exist in the brain and receive descending commands from a variety of cortical and subcortical structures involved in limbic (emotional) systems. However, it remains unclear how the lateral habenula (LHb), a center of negative emotions (e.g., pain, stress and anxiety), can influence the control of jaw movements. To address this issue, we examined whether and how the LHb directly projects to the Vmes by means of neuronal tract tracing techniques in rats. After injections of a retrograde tracer Fluorogold in the rostral and caudal Vmes, a number of neurons were labeled in the lateral division of LHb (LHbl) bilaterally, whereas a few neurons were labeled in the medial division of LHb (LHbm) bilaterally. After injections of an anterograde tracer, biotinylated dextranamine (BDA) in the LHbl, a small number of labeled axons were distributed bilaterally in the rostral and caudal levels of Vmes, where some labeled axonal boutons contacted the cell body of rostral and caudal levels of Vmes neurons bilaterally. After the BDA injection into the LHbm, however, no axons were labeled bilaterally in the rostral and caudal levels of Vmes. Therefore, the present study for the first time demonstrated the direct projection from the LHbl to the Vmes and the detailed projection patterns, suggesting that jaw movements are modulated by negative emotions that are signaled by LHbl neurons.
Generation of the masticatory central pattern and its modulation by sensory feedback
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The basic pattern of rhythmic jaw movements produced during mastication is generated by a neuronal network located in the brainstem and referred to as the masticatory central pattern generator (CPG). This network composed of neurons mostly associated to the trigeminal system is found between the rostral borders of the trigeminal motor nucleus and facial nucleus. This review summarizes current knowledge on the anatomical organization, the development, the connectivity and the cellular properties of these trigeminal circuits in relation to mastication. Emphasis is put on a population of rhythmogenic neurons in the dorsal part of the trigeminal sensory nucleus. These neurons have intrinsic bursting capabilities, supported by a persistent Na⁺ current (I_NaP), which are enhanced when the extracellular concentration of Ca²⁺ diminishes. Presented evidence suggest that the Ca²⁺ dependency of this current combined with its voltage-dependency could provide a mechanism for cortical and sensory afferent inputs to the nucleus to interact with the rhythmogenic properties of its neurons to adjust and adapt the rhythmic output. Astrocytes are postulated to contribute to this process by modulating the extracellular Ca²⁺ concentration and a model is proposed to explain how functional microdomains defined by the boundaries of astrocytic syncitia may form under the influence of incoming inputs.
Direct projections from the central amygdaloid nucleus to the mesencephalic trigeminal nucleus in rats
2011, Brain Research
Citation Excerpt :
The terminal buttons on Me5 somata were concentrated in the caudal part of the nucleus and the number of buttons per soma was also higher in the caudal part of the Me5. Previous research has indicated that proprioceptive signals from the periodontal ligament are restricted to neurons in the caudal part of the Me5 in the rat (Gonzálo-Sanz and Insausti, 1980) and cat (Nomura and Mizuno, 1985). In contrast, proprioceptive signals from the muscle spindles of the masticatory muscles are distributed throughout the nucleus (Nomura and Mizuno, 1985).
The amygdala is activated by fear and plays an important role in the emotional response to life-threatening situations. When rats feel threatened, they respond by biting fiercely. Bite strength is regulated by the trigeminal motor nucleus and the mesencephalic trigeminal nucleus (Me5). The Me5 relays proprioceptive signals from the masticatory muscles and the periodontal ligaments to the trigeminal motor and premotor nuclei. The amygdala projects to the trigeminal motor nucleus and the premotor reticular formation. However, it is unknown whether the amygdala projects directly to the Me5. In the present study, neurons of the central amygdaloid nucleus (ACe) were labeled following injection of a retrograde tracer, Fast Blue, into the caudal Me5, and fibers and terminal buttons from the ACe to the Me5 were examined after injections of an anterograde neuronal tracer, biotinylated dextran amine into the ACe. Furthermore, wheat germ agglutinin-conjugated to horseradish peroxidase was injected into the ACe, and labeled fibers and terminal buttons in the Me5 were examined by electron microscopy. Labeled terminal buttons on Me5 somata were more abundant in the caudal than the rostral Me5. Electron microscopic observation revealed that a part of these terminal buttons formed axo-somatic synapses. These results indicate that the ACe sends direct projections to the Me5, and suggest that the amygdala regulates bite strength by modifying neuronal activity in the Me5.
Corticofugal direct projections to primary afferent neurons in the trigeminal mesencephalic nucleus of rats
2010, Neuroscience
Citation Excerpt :
In the present study, the Agm, ACg, PrL and IL projected rostrocaudally to all levels of the Vmes, while the DP and Ins projected almost exclusively to the caudal level of Vmes, indicating that the Vmes neurons receive topographic projections from the prefrontal cortex. It is well known that the somata of Vmes neurons innervating the masticatory muscle spindles are located throughout the Vmes, while those innervating the periodontal ligaments are located only in its caudal half (rat, Gonzálo-Sanz and Insausti, 1980; Zhang et al., 1992; cat, Jerge, 1963; Cody et al., 1972; Linden, 1978; Gottlieb et al., 1984; Nomura and Mizuno, 1985). Therefore, the present results suggest that the spindle Vmes neurons in the rostral Vmes receive more inputs from the Agm, ACg, PrL and IL, and that the periodontal Vmes neurons receive more inputs from the DP and Ins.
Little is known about projections from the cerebral cortex to the trigeminal mesencephalic nucleus (Vmes) which contains the cell bodies of primary sensory afferents innervating masticatory muscle spindles and periodontal ligaments of the teeth. To address this issue, we employed retrograde (Fluorogold, FG) and anterograde (biotinylated dextranamine, BDA) tracing techniques in the rat. After injections of FG into the Vmes, a large number of neurons were retrogradely labeled in the prefrontal cortex including the medial agranular cortex, anterior cingulate cortex, prelimbic cortex, infralimbic cortex, deep peduncular cortex and insular cortex; the labeling was bilateral, but with an ipsilateral predominance to the injection site. Almost no FG-labeled neurons were found in the somatic sensorimotor cortex. After BDA injections into the prefrontal cortex, anterogradely labeled axon fibers and boutons were distributed bilaterally in a topographic pattern within the Vmes, but with an ipsilateral predominance to the injection site. The rostral Vmes received more preferential projections from the medial agranular cortex, while the deep peduncular cortex and insular cortex projected more preferentially to the caudal Vmes. Several BDA-labeled axonal boutons made close associations (possible synaptic contacts) with the cell bodies of Vmes neurons. The present results have revealed the direct projections from the prefrontal cortex to the primary sensory neurons in the Vmes and their unique features, suggesting that deep sensory inputs conveyed by the Vmes neurons from masticatory muscle spindles and periodontal ligaments are regulated with specific biological significance in terms of the descending control by the cerebral cortex.
The intermedius nucleus of the medulla: A potential site for the integration of cervical information and the generation of autonomic responses
2009, Journal of Chemical Neuroanatomy
The intermedius nucleus of the medulla (InM) is a small perihypoglossal brainstem nucleus, which receives afferent information from the neck musculature and also descending inputs from the vestibular nuclei, the gustatory portion of the nucleus of the solitary tract (NTS) and cortical areas involved in movements of the tongue. The InM sends monosynaptic projections to both the NTS and the hypoglossal nucleus. It is likely that the InM acts to integrate information from the head and neck and relays this information on to the NTS where suitable autonomic responses can be generated, and also to the hypoglossal nucleus to influence movements of the tongue and upper airways.
Central to the integratory role of the InM is its neurochemical diversity. Neurones within the InM utilise the amino acid transmitters glutamate, GABA and glycine. A proportion of these excitatory and inhibitory neurones also use nitric oxide as a neurotransmitter. Peptidergic transmitters have also been found within InM neurones, although as yet the extent of the pattern of co-localisation between peptidergic and amino acid transmitters in neurones has not been established.
The calcium binding proteins calretinin and parvalbumin are found within the InM in partially overlapping populations. Parvalbumin and calretinin appear to have complementary distributions within the InM, with parvalbumin being predominantly found within GABAergic neurones and calretinin being predominantly found within glutamatergic neurones.
Neurones in the InM receive inputs from glutamatergic sensory afferents. This glutamatergic transmission is conducted through both NMDA and AMPA ionotropic glutamate receptors.
In summary the InM contains a mixed pool of neurones including glutamatergic and GABAergic in addition to peptidergic neurones. Neurones within the InM receive inputs from the upper cervical region, descending inputs from brain regions involved in tongue movements and those involved in the co-ordination of the autonomic nervous system. Outputs from the InM to the NTS and hypoglossal nucleus suggest a possible role in the co-ordination of tongue movements and autonomic responses to changes in posture.

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^*: Present address: College of Medical Technology, Kyoto University, Kyoto 606 (Japan)

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Differential distribution of cell bodies and central axons of mesencephalic trigeminal nucleus neurons supplying the jaw-closing muscles and periodontal tissue: A transganglionic tracer study in the cat

Brain Research

Exp. Neurol.

Neurosci. Lett.

Exp. Neurol.

Exp. Neurol.

Neurosci. Lett.

Exp. Neurol.

Neurosci. Lett.

Brain Research

Exp. Neurol.

Brain Research

Brain Research

Exp. Neurol.

Mesencephalic projections of the rectus lateralis muscle afferents in the cat

Arch. Ital. Biol.

The projection of jaw elevator muscle spindle afferents to fifth nerve motoneurones in the cat

J. Physiol. (London)

Retrograde cellular changes in the mesencephalic trigeminal nucleus in the cat following cerebellar lesions

Acta Morphol. Neerl.-Scand.

Distribution of tooth receptor afferents in the mesencephalic nucleus of the fifth cranial nerve

J. Physiol. (London)

A functional analysis of the components of the mesencephalic nucleus of the fifth nerve in the cat

J. Physiol. (London)

Nerve impulses in the brainstem of the goat: short latency responses obtained by stretching the extrinsic eye muscles and jaw muscles

J. Physiol. (London)

Observations on the peripheral distribution of fibres arising in the mesencephalic nucleus of the fifth cranial nerve

J. Comp. Neurol.

Function of mesencephalic root of fifth cranial nerve

J. Neurophysiol.

A trigeminal midbrain-cerebellar fiber connection in the rat

J. Comp. Neurol.

Axon morphology of mesencephalic trigeminal neurons in a snake

Thamnophis sirtalis, J. Comp. Neurol.

Projections of the optic tectum and the mesencephalic nucleus of the trigeminal nerve in the tegulizard (Upinabis nigropunctatus)

Cell Tissue Res.

Responses in the brainstem of the cat to stretch of extrinsic ocular muscles

J. Physiol. (London)

The distribution of afferent neurones in the mesencephalic nucleus of the fifth nerve in the cat

J. Comp. Neurol.