Two types of jaw-muscle spindle afferents in the cat as demonstrated by intra-axonal staining with HRP

doi:10.1016/0006-8993(90)91418-G

Brain Research

Volume 514, Issue 2, 30 April 1990, Pages 219-237

https://doi.org/10.1016/0006-8993(90)91418-G Get rights and content

Abstract

Intra-axonal records and horseradish peroxidase (HRP) injection techniques were employed to define the response properties of the jaw-closing muscle spindle afferents in the trigeminal mesencephalic nucleus (Vmes) and their morphological characteristics. The axonal trajectories of 9 spindle afferents from the masseter and 4 afferents from the temporalis were recovered for detailed analyses. Of 13 afferents, 6 cell bodies were stained and they were located at the rostrocaudal mid-levels of the Vmes. The central courses of the stem fibers were organized in a similar manner to the Vmes periodontal afferent nerves³⁰ with the exception that peripheral (P) fibers of all spindle afferents passed through the trigeminal motor tract and root. On the basis of collateral terminal arborizations, the Vmes spindle afferents could be classified into two types: type I (n = 6) and type II (n = 7). Type I afferents sent their collaterals into the trigeminal motor nucleus (Vmo), intertrigeminal region (Vint) and juxtatrigeminal region (Vjux), but collaterals from the two neurons also projected to Vmes and the nucleus oralis (Vo). The collaterals from type II afferents formed their terminal arbors in the supratrigeminal nucleus (Vsup) in addition to the Vmo, Vint and Vjux, but collaterals from one neuron also projected to the Vo. In type I afferents, terminal arbors encompassed the whole Vmo including jaw-closing motoneurons. In contrast, boutons from type II afferents were restricted to a few small portions within the Vmo in proximity to its lateral and dorsal boundaries. The diameters of the united (U), central (C) and peripheral (P), fibers were larger in type I than type II afferents; those of the U fibers were statistically significant. Any differences between the two distinct types were not found in the response pattern to the sustained jaw opening. These results suggest that the difference of primary and secondary muscle-spindle afferent nerves is reflected in a distinctive morphology in the terminal arborizations and in the diameters of united fibers rather than the response patterns in deeply anesthetized cats.

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Meanwhile, we also conducted electrophysiological single unit recording in the III and INC by electric stimuli on the rat masseter nerve, and we recorded some orthodromic unit discharges in the III and INC [63]. Hence, we considered this pathway is mainly composed of jaw muscle afferent Vme because their peripheral processes travel through the masseter nerve [64,65]; in contrast, peripheral process of the periodontal afferent Vme neurons do not. Further, we also visualized intracellularly labeled axons of the jaw muscle afferent Vme neuron climbing into the ipsilateral III following injection of tracers into a Vme neuronal soma that responds to electric stimuli of the masseter nerve [62].
Marcus Gunn Syndrome (MGS), mostly occurring in congenital ptosis patients, is characterized by jaw movement evoking ptotic eyelid retraction, followed by collapse. Inverted, bilateral and acquired MGS were also reported. Some cases manifest MGS only temporarily in life. These features suggest MGS may be due to multiple pathogeneses, which are still unclear. People also classify MGS as a kind of trigeminal oculomotor synkenesis (TOS), like Duane syndrome (DS), in which ocular adduction prompts eyelid moving or eyeball retraction. The most popular hypothesis for TOS is congenital miswiring, as evidence supporting this hypothesis is found in DS cases: hypoplasia abducens nerve fusing with a branch of oculomotor nerve is observed. Seven mutant genes have been identified associated with TOS and two of them are found among MGS cases. Accordingly, these mutant genes may dominate cranial nerve misconnection and generate TOS. However, unlike in DS case, evidence of miswiring is not encountered in most MGS cases. The fact is that two “MGS genes” are from congenital fibrosis of extraocular muscle (CFEOM) cases presenting with associated MGS. But most of MGS cases do not suffer CFEOM. Thus, mutant genes dominated congenital miswiring may not be the pathogenesis for the majority of MGS. As an alternate pathogenic pathway, a “release hypothesis” proposed that MGS is a primitive physiologic reflex that became suppressed during phylogenetic development but could be released under certain pathologic conditions. This hypothesis was and is overlooked because the hypothesized reflex arc has not been defined. Decades ago, a neural tract tracing study in Xenopus revealed a direct projection from masticator afferent mesencephalic trigeminal nucleus (Vme) neurons to oculomotor and trochlear nucleus (III/IV). In clinical studies, co-firing of pterygoid muscle and levator palpebrae was recorded by electromyography during onset of MGS, and stimulating pterygoid muscle nerve elicited eyelid retraction. Recently, retraction of the ipsilateral eyelid by stimulating the trigeminal motor root was even observed in cases without congenital ptosis and MGS, highlighting the existence of a latent pathway. In rats, recently we demonstrated projections from the Vme neurons to the III/IV, and to their premotor neurons in interstitial nucleus of Cajal by neural tract tracing and electrophysiologic studies. Fos expression in pre-oculomotor neurons was induced by repeated down stretching the lower jaw. Combining previous and our own studies, we assumed the Vme neurons is excited when jaw moves and in turn, some eyelid activity related III motoneurons are activated through projections of Vme to oculomotor system, like in Xenopus. Genetic factors may dominate to what extent this primitive reflex-arc is preserved, which consequently determines phenotype.
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We have recently revealed that the proprioceptive signal from jaw-closing muscle spindles (JCMSs) is conveyed to the dorsal part of granular insular cortex rostroventrally adjacent to the rostralmost part of secondary somatosensory cortex (dGIrvs2) via the caudo-ventromedial edge (VPMcvm) of ventral posteromedial thalamic nucleus (VPM) in rats. However, it remains unclear to which cortical or subcortical structures the JCMS proprioceptive information is subsequently conveyed from the dGIrvs2. To test this issue, we injected an anterograde tracer, biotinylated dextranamine, into the electophysiologically identified dGIrvs2, and analyzed the resultant distribution profiles of labeled axon terminals in rats. Labeled terminals were distributed with an ipsilateral predominance. In the cerebral cortex, they were seen in the primary and secondary somatosensory cortices, lateral and medial agranular cortices and dorsolateral orbital cortex. In the basal ganglia, they were found in the caudate putamen, core part of accumbens nucleus, lateral globus pallidus, subthalamic nucleus, and substantia nigra pars compacta and pars reticulata. They were also observed in the central amygdaloid nucleus and extended amygdala (the interstitial nucleus of posterior limb of anterior commissure and the juxtacapsular part of lateral division of bed nucleus of stria terminalis). In the thalamus, they were seen in the reticular nucleus, ventromedial nucleus, core VPM, parvicellular part of ventral posterior nucleus, oval paracentral nucleus, medial and triangular parts of posterior nucleus, and zona incerta as well as the VPMcvm. These data suggest that the JCMS proprioceptive information through the dGIrvs2 is transmitted to the emotional ‘limbic’ regions as well as sensorimotor regions.
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Citation Excerpt :
Intraaxonal labeling studies have revealed that the rat spindle Me5 afferents ipsilaterally project not only to jaw-closing motoneurons in the trigeminal motor nucleus (Mo5) but also to pontomedullary regions such as the supratrigeminal nucleus (Su5), dorsomedial part of the trigeminal principal nucleus (Pr5) and dorsomedial part of trigeminal oral subnucleus (5Odm); these regions contain premotoneurons projecting to the Mo5 bilaterally with an ipsilateral predominance (Luo et al., 1995, 2001). These earlier findings indicate that the JCMS proprioceptive information can directly or indirectly exert reflexive jaw-movements (Goldberg and Nakamura, 1968; Kidokoro et al., 1968; Ohta and Moriyama, 1986; Shigenaga et al., 1988, 1990). We have recently demonstrated that the rat JCMS proprioceptive signals through the spindle Me5 afferents are conveyed to the Su5, then to the caudo-ventromedial edge (VPMcvm) of the ventral posteromedial thalamic nucleus (VPM) on the contralateral side, and finally to the dorsal part (dGIrvs2) of granular insular cortex (GI) rostroventrally adjacent to the rostralmost part of secondary somatosensory cortex (S2) (Fujio et al., 2016; Sato et al., 2017; Yoshida et al., 2017).
Our motor behavior can be affected by proprioceptive information. However, little is known about which brain circuits contribute to this process. We have recently revealed that the proprioceptive information arising from jaw-closing muscle spindles (JCMSs) is conveyed to the supratrigeminal nucleus (Su5) by neurons in the trigeminal mesencephalic nucleus (Me5), then to the caudo-ventromedial edge of ventral posteromedial thalamic nucleus (VPMcvm), and finally to the dorsal part of granular insular cortex rostroventrally adjacent to the rostralmost part of secondary somatosensory cortex (dGIrvs2). Our next question is which brain areas receive the information from the dGIrvs2 for the jaw-movements. To test this issue, we injected an anterograde tracer, biotinylated dextranamine, into the dGIrvs2, and analyzed the resultant distribution profiles of the labeled axon terminals. Anterogradely labeled axons were distributed in the pontomedullary areas (including the Su5) which are known to receive JCMS proprioceptive inputs conveyed directly by the Me5 neurons and to contain premotoneurons projecting to the jaw-closing motoneurons in the trigeminal motor nucleus (Mo5). They were also found in and around the VPMcvm. In contrast, no labeled axonal terminals were detected on the cell bodies of Me5 neurons and motoneurons in the Mo5. These data suggest that jaw-movements, which are evoked by the classically defined jaw-reflex arc originating from the peripheral JCMS proprioceptive information, could also be modulated by the transcortical feedback connections from the dGIrvs2 to the VPMcvm and Su5.
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Little is known about how proprioceptive signals arising from muscles reach to higher brain regions such as the cerebral cortex. We have recently shown that a particular thalamic region, the caudo-ventromedial edge (VPMcvm) of ventral posteromedial thalamic nucleus (VPM), receives the proprioceptive signals from jaw-closing muscle spindles (JCMSs) in rats. In this study, we further addressed how the orofacial thalamic inputs from the JCMSs were transmitted from the thalamus (VPMcvm) to the cerebral cortex in rats. Injections of a retrograde and anterograde neuronal tracer, wheat-germ agglutinin-conjugated horseradish peroxidase (WGA-HRP), into the VPMcvm demonstrated that the thalamic pathway terminated mainly in a rostrocaudally narrow area in the dorsal part of granular insular cortex rostroventrally adjacent to the rostralmost part of the secondary somatosensory cortex (dGIrvs2). We also electrophysiologically confirmed that the dGIrvs2 received the proprioceptive inputs from JCMSs. To support the anatomical evidence of the VPMcvm–dGIrvs2 pathway, injections of a retrograde neuronal tracer Fluorogold into the dGIrvs2 demonstrated that the thalamic neurons projecting to the dGIrvs2 were confined in the VPMcvm and the parvicellular part of ventral posterior nucleus. In contrast, WGA-HRP injections into the lingual nerve area of core VPM demonstrated that axon terminals were mainly labeled in the core regions of the primary and secondary somatosensory cortices, which were far from the dGIrvs2. These results suggest that the dGIrvs2 is a specialized cortical region receiving the orofacial proprioceptive inputs. Functional contribution of the revealed JCMSs–VPMcvm–dGIrvs2 pathway to Tourette syndrome is also discussed.
Direct projection from the lateral habenula to the trigeminal mesencephalic nucleus in rats
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Citation Excerpt :
Many Vmes neurons in all vertebrates have been reported to make soma-somatic contacts that are considered to be sites for electric coupling between the Vmes neurons (Baker and Llinás, 1971; Hinrichsen and Larramendi, 1968, 1969, 1979; Liem et al., 1991; Rokx and van Willigen, 1988). It has also been demonstrated that some Vmes neurons give off axon collaterals terminating the cell bodies of other Vmes neurons (Dessem and Taylor, 1989; Luo and Dessem, 1996; Luo et al., 1995; Paik et al., 2005; Shigenaga et al., 1990). These earlier findings suggest the possibility that the Vmes neurons can activate the neighboring Vmes neurons by local interneuronal connections; thus, the activation of a small number of Vmes cells can exert spreading effects on a large number of Vmes cells to powerfully modulate jaw movements.
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.
Jaw muscle spindle afferents coordinate multiple orofacial motoneurons via common premotor neurons in rats: An electrophysiological and anatomical study
2012, Brain Research
Jaw muscle spindle afferents (JMSA) in the mesencephalic trigeminal nucleus (Vme) project to the parvocellular reticular nucleus (PCRt) and dorsomedial spinal trigeminal nucleus (dm-Vsp). A number of premotor neurons that project to the trigeminal motor nucleus (Vmo), facial nucleus (VII) and hypoglossal nucleus (XII) are also located in the PCRt and dm-Vsp. In this study, we examined whether these premotor neurons serve as common relay pool for relaying JMSA to multiple orofacial motoneurons. JMSA inputs to the PCRt and dm-Vsp neurons were verified by recording extracellular responses to electrical stimulation of the caudal Vme or masseter nerve, mechanical stimulation of jaw muscles and jaw opening. After recording, biocytin in recording electrode was inotophorized into recording sites. Biocytin-Iabeled fibers traveled to the Vmo, VII, XII, and the nucleus ambiguus (Amb). Labeled boutons were seen in close apposition with Nissl-stained motoneurons in the Vmo, VII, XII and Amb. In addition, an anterograde tracer (biotinylated dextran amine) was iontophorized into the caudal Vme, and a retrograde tracer (Cholera toxin B subunit) was delivered into either the VII or Xll to identify VII and XII premotor neurons that receive JMSA input. Contacts between labeled Vme neuronal boutons and premotor neurons were observed in the PCRt and adjacent dm-Vsp. Confocal microscopic observations confirmed close contacts between Vme boutons and VII and XII premotor neurons. This study provides evidence that JMSA may coordinate activities of multiple orofacial motor nuclei, including Vmo, VII, XII and Amb in the brainstem via a common premotor neuron pool.

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Two types of jaw-muscle spindle afferents in the cat as demonstrated by intra-axonal staining with HRP

Abstract

Technical considerations on the use of horseradish peroxidase as a neuronal maker

Neuroscience

Morphological and electrophysiological determination of the projections of jaw-elevator muscle spindle afferents in rats

J. Physiol. (Lond.)

On the central course of afferent fibers in the trigeminal, facial, glossopharyngeal, and vagal nerves and their nuclei in the mouse

Acta Physiol. Scand.

The morphology of Group Ia afferent fiber collaterals in the spinal cord of the cat

J. Physiol. (Lond.)

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

J. Physiol. (Lond.)

Morphology of jaw-muscle spindle afferents in the rat

J. Comp. Neurol.

The morphology of Group II muscle afferent fiber collaterals

J. Physiol. (Lond.)

Response characteristics and classification of muscle spindles of the masseter muscle in the cat

Exp. Neurol.

Trajectory of group Ia afferent fibers strained with horseradish peroxidase in the lumbosacral spinal cord of the cat: three-dimensional reconstructions from serial sections

J. Comp. Neurol.

Organization and function of the trigeminal mesencephalic nucleus

J. Neurophysiol.

The function of the nucleus supratrigeminalis

J. Neurophysiol.

Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat

J. Comp. Neurol.

Bulbar neurons with axonal projections to the trigeminal motor nucleus in the cat

Exp. Brain Res.

Jaw muscle afferent firing during an isotonic jaw-positioning task in the monkey

J. Neurophysiol.

Discharge characteristics and stretch sensitivity of jaw muscle afferents in the monkey during controlled isometric bites

J. Neurophysiol.

Contribution al concimento del nervio trigemino

Quantitative analysis of the morphology of group II fibers in the spinal cord of the cat

Neurosci. Lett.

Peripheral and central distribution of fibers of the mesencephalic trigeminal root in the rat

Neurosci. Lett.

A Cytoarchitectonic Atlas of the Rhombencephalon of the Rabbit

Terminals of Ia fibers: location, density and distribution within a pool of 300 homonymous motoneurons

J. Neurophysiol.