Yoshio Shigenaga

The distribution of muscle primary afferents from the masseter nerve to the trigeminal sensory nuclei

Transganglionic transport of horseradish peroxidase--wheat germ agglutinin conjugate was used to study the pattern of termination of somatic afferent fibers innervating the masseter muscle within the trigeminal sensory nuclear complex (TSNC) of the cat. The central processes of the masseteric nerve terminated in the caudal third of the pars interpolaris, and laminae I/V through the caudal two-thirds of caudalis and rostral parts of the C1 spinal cord segment. The functional significance of the masseteric afferent projections to the TSNC with a preferential pattern was discussed, particularly with respect to muscle pain.

Physiological and morphological characteristics of cat masticatory motoneurons--intracellular injection of HRP.

The physiology and morphology of masticatory motoneurons of adult cats were examined by the methods of intracellular recording and intracellular injection of horseradish peroxidase. Masseter and jaw-opening motoneurons were identified by intracellular recordings of the antidromic response following stimulation of the masseter and mylohyoid nerves, respectively. An excitatory postsynaptic potential (EPSP) was recorded from masseter neurons by stimulation of the masseter nerve with stimulus intensity below threshold for antidromic response. In contrast, the EPSP was not recorded from jaw-opening motoneurons by stimulation of the mylohyoid nerve with stimulus intensity below threshold for antidromic response. Patterns of postsynaptic potentials (PSPs) in the masseter motoneurons following stimulation of the tooth pulp or periodontal afferents were classified into 4 types: hyperpolarization (n = 40), depolarization-hyperpolarization (n = 9), hyperpolarization-depolarization (n = 5), and depolarization with spike potentials (n = 10). On the other hand, patterns of the PSPs in the jaw-opening motoneurons following stimulation of the same afferents were classified into two types: depolarization with spike potentials (n = 19), and hyperpolarization (n = 5). Twenty-five masseter and 7 jaw-opening motoneurons and an intranuclear neuron were reconstructed from serial sections in the transverse plane. On the basis of dendritic morphology, the masseter motoneurons could be classified into two major groups, type I (n = 15) and type II (n = 9), whereas two neurons were found to constitute a separate category of the masseter motoneuron. The dendritic distributions of all the jaw-opening motoneurons examined were generally similar and there was no indication of the existence of subtypes, whereas there were 2 or 3 subgroups in type I and type II masseter motoneurons. Type I masseter neurons had primary dendrites which extended radially in all directions, and the whole profile of their dendritic trees presented a spherical and an egg-shaped appearance. In type II masseter neurons, the origin of primary dendrites was bipolar or tripolar, and the whole profile of their dendritic trees presented a hemispherical and mirror-imaged, funnel-shaped appearance. The other two masseter motoneurons had a particular dendritic tree which was much simpler in configuration, with less tapering or branching than those of other neurons examined. In contrast, the dendritic profiles of all the jaw-opening motoneurons were similarly organized and showed vertically oriented dendritic trees which were more developed in the dorsomedial than in the ventrolateral direction.(ABSTRACT TRUNCATED AT 400 WORDS)

Physiological and morphological characteristics of periodontal mesencephalic trigeminal neurons in the cat — intra-axonal staining with HRP

Intra-axonal recording and horseradish peroxidase (HRP) injection techniques were employed to define the response properties of periodontal mechanoreceptive afferents originating from the trigeminal mesencephalic nucleus (Vmes) and their morphological characteristics. The periodontal Vmes neurons were classified into two types: slowly adapting (SA) and fast adapting (FA) types. The central terminals of 7 SA and 4 FA afferents were recovered for detailed analyses. The whole profile of SA and FA neurons were unipolar in shape and their cell bodies were located in the dorsomedial parts of the Vmes. The united (U) fiber traveled caudally from the soma to the dorsolateral aspect of the trigeminal motor nucleus (Vmo), where it split into the peripheral (P) and C fibers with a T- or Y-shaped appearance. The P fiber joined the trigeminal sensory or motor tract. The C fiber descended caudally within Probsts tract. All 3 stem fibers issued main collaterals. The main collaterals of all neurons examined formed terminal arbors in the supratrigeminal nucleus (Vsup) and all but two SA neurons projected to the intertrigeminal region (Vint), while the projections to other nuclei of the trigeminal motor nucleus (Vmo), juxtatrigeminal region (Vjux), main sensory nucleus (Vp) and oral nucleus (Vo.r) differed between SA and FA afferents and between neurons of the same type. The SA and FA neurons were classified into three and two subgroups, respectively. The major differences in central projections between the two types were that all the FA neurons projected to the Vp or Vo.r but none of SA type and this relation was reversed in the projection to the Vjux, and that more than half of SA neurons projected to Vmo but only one FA neuron to the Vmo. The Vmes neurons which sent their collaterals into the Vmo had the P fiber passing through the tract of the trigeminal motor nerve. The average size of somata and mean diameters of U fibers and main collaterals from C fiber were significantly larger in SA neurons than FA neurons. The average size of fiber varicosities became smaller in the following nuclei, Vmo, Vsup, Vp, Vint and Vo.r, but not significant between the two functional types. The functional role of the periodontal Vmes afferents to jaw reflexes was discussed particularly with respect to their central projection sites in the brainstem nuclei.

Morphology of single mesencephalic trigeminal neurons innervating masseter muscle of the cat

The morphology of functionally identified single axons of mesencephalic trigeminal neurons was studied in the cat by the method of intra-axonal injection of horseradish peroxidase (HRP). Each axon can be divided into united (U), peripheral (P) and central branches (C). The united axon (U) descends from its soma within the tract of the trigeminal mesencephalic nucleus to the dorsal aspect of the trigeminal motor nucleus (Vmo), where it splits into peripheral and descending central branches with a Y-shaped bifurcation. The peripheral axon (P) joins the motor root of the trigeminal nerve to exit the brainstem. The central axon (C) travels caudally within the juxtatrigeminal regions (or lateral reticular formation). All 3 branches issue axon collaterals that distribute terminal boutons within the dorsolateral subdivision of Vmo, supra- and intertrigeminal regions. Collaterals emanating from the central axon (C) except for its proximal segment travel ventrolaterally within the juxtatrigeminal regions, and send their terminal branches into the lateral boundaries adjacent to the spinal trigeminal nucleus. The trajectory of terminal branches distinguishes group Ia afferents from the possible group II afferents. The majority of terminal boutons are found to distribute in the supra- and intertrigeminal regions for group II afferent fibers and in the dorsolateral subdivision of Vmo for group Ia afferents.

Ascending and descending internuclear projections within the trigeminal sensory nuclear complex

The cells of origin of ascending and descending internuclear pathways in the trigeminal sensory nuclear complex were studied by the method of retrograde transport of horseradish peroxidase in the cat. The cells of origin of the ascending internuclear pathways are distributed in all laminae of the caudal part of the spinal trigeminal nucleus (Vc) except for lamina II and the caudal regions of the pars interpolaris of the spinal trigeminal nucleus (Vi). The cells arising from the Vc project to all rostral trigeminal nuclei except the caudal Vi and dorsal part of the principal trigeminal nucleus (Vpd), and neurons of the caudal Vi project to the dorsomedial (Vo.dm) and rostrodorsomedial (Vo.r) divisions of the spinal trigeminal nucleus and the ventral part of the principal trigeminal nucleus (Vpv), although the main ascending fibers from the Vc arise from laminae III-V and project to the rostral Vi and pars oralis. By contrast, the cells of origin of the descending internuclear pathways are distributed in all trigeminal nuclei, with chain-like connections between the neighboring nuclei, while the caudal regions of the Vi and laminae I-II do not receive any descending projections. The main ascending fibers from the paratrigeminal nucleus (or interstitial nucleus) at the caudal level of the Vi project to the parabrachial nucleus. These findings indicate that the internuclear pathways are differentially organized between the ascending and descending projections, and suggest that the internuclear trigeminal connections have a smaller influence on the trigeminothalamic tract cells in the Vpd, caudal Vi, and lamina I.

Somatotopic organization of tooth pulp primary afferent neurons in the cat

Transganglionic transport of horseradish peroxidase-wheat germ agglutinin conjugate (HRP-WGA) was used to study the somatotopic organization of pulpal afferent neurons innervating the different types of teeth in the trigeminal ganglion and trigeminal sensory nuclear complex (TSNC). In separate animals, the upper first 3 incisors (UI1-3), canine (UC), second premolar (UP2) and third premolar (UP3), and the lower first three incisors (LI1-3), canine (LC), first premolar (LP1), second premolar (LP2) and molar (LM) were traced in this experiment. Cell bodies innervating posterior teeth were found with greater frequency in dorsal maxillary ganglion regions, while somata supplying more anterior teeth were predominant ventrally. In contrast, cell bodies innervating the lower teeth were not arranged in a somatotopic fashion in the mandibular subdivision. Each pulpal afferent from lower and upper teeth projected to the subnucleus dorsalis (Vpd) of the pars principalis, the rostrodorsomedial (Vo.r) and dorsomedial parts (Vo.dm) of the pars oralis (Vo), the medial regions of the pars interpolaris (Vi), and laminae I, II, and V of the medullary dorsal horn, and terminal fields between the upper and lower teeth were separated in each subdivision. Pulpal projections from both the upper and lower teeth to each subdivision were organized in a somatotopic manner, while an extensive overlap in projections was noted between the adjoining teeth. In the Vpd, the upper and lower teeth were represented dorsoventrally, and projections from the anterior to posterior teeth in the upper jaw were arranged in both rostrocaudal and ventrodorsal sequences whereas those in the lower jaw were organized caudarostrally and lateromedially. In the Vo.r and Vo.dm, the upper and lower teeth were represented in a mediolateral sequence and projections from the anterior to posterior teeth were organized in a ventrolateral to dorsomedial sequence. In the Vi, pulpal projections were organized in a topographic fashion similar to that observed in the Vo.r and Vo.dm. In the medullary dorsal horn, the upper and lower teeth were represented in laminae I, II and V in a lateromedial sequence. Their projections to laminae I and V were topographically organized in a mediolateral and rostrocaudal sequence.(ABSTRACT TRUNCATED AT 400 WORDS)

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

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 nerves 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.

Morphology of single mesencephalic trigeminal neurons innervating periodontal ligament of the cat

The morphology of single neurons in the trigeminal mesencephalic nucleus (Vmes) that innervate periodontal ligament was studied in cats by the method of intraaxonal injection of horseradish peroxidase (HRP). Two kinds of Vmes neurons were distinguished on the basis of differences in axon profile and its central projection. The first type of Vmes neurons was unipolar in shape and its axon was divided into united (U), peripheral (P), and central axons (C). The U axon traveled caudally within the Vmes from the soma to the dorsolateral aspect of trigeminal motor nucleus (Vmo), where it split into the P and C axons with a T-shaped appearance. The P axon joined the spinal trigeminal tract across the trigeminal principal nucleus and ran within the tract and sensory root to exit the brainstem. The C axon traveled caudally within Probsts tract. All 3 axons issued axon collaterals. Axon collaterals from the U, P and the proximal C axons sent their terminal branches into the supra (Vsup) and intertrigeminal regions (Vint). Most axon collaterals from the C axon sent their terminal branches into the juxtatrigeminal regions (Vjuxta). The second type of Vmes neurons was bipolar and issued P and C axons. The C axon ran a short distance in the Vmes to leave the Vmes, and then it traveled caudolaterally in the rostrodorsomedial aspect of the Vmo. Finally, it entered in the Vmo and traveled caudally in the dorsolateral subdivision of the nucleus to its rostrocaudal mid-level. The C axon gave off massive axon collaterals.(ABSTRACT TRUNCATED AT 250 WORDS)

Central terminations of periodontal mechanoreceptive and tooth pulp afferents in the trigeminal principal and oral nuclei of the cat.

Intra-axonal recording and horseradish peroxidase (HRP) injection techniques were employed to define the response properties of low-threshold mechanoreceptive periodontal afferents and of the tooth pulp afferents and the morphological characteristics of their axon arbors in the nucleus principalis (Vp) and rostrodorsomedial (Vo.r) and dorsomedial parts (Vo.dm) of the nucleus oralis (Vo). The central terminals of 3 fast adapting (FA) and 4 slowly adapting (SA) periodontal afferents and 4 tooth pulp (TP) afferents were recovered for detailed analyses. Stained axons in the trigeminal sensory tract ascended and descended (bifurcating fibers), or descended without bifurcation (descending non-bifurcating fibers). The ratio of the bifurcating fibers to the descending non-bifurcating fibers was about three to one for each type of afferents. The main collaterals given off from the ascending branches terminated in the Vp. Most collaterals given off from the descending branches terminated in the Vo with the exception of few instances. In case of the FA afferents, the ascending branches gave off all main collaterals into the Vp with rostrocaudal and dorsoventral continuities in their arbors, whereas the descending branches gave off all main collaterals, except two collaterals, into the Vo with rostrocaudal discontinuities. The projections from the FA afferents to the Vo.dm was predominant in terms of the number of boutons and the length of preterminal and terminal branches. In case of the SA afferents, the collaterals from the ascending and descending branches formed rostrocaudally and dorsoventrally discontinuous terminal arbors. In terms of the density of boutons the SA afferents were divided into two subtypes. One had a preferential projection into the Vp or Vo, whereas others lacked a selective projection. In case of the TP afferents, the main collaterals of the ascending branches formed partially overlapping terminal arbors, but the terminal arbors formed by the collateral of the descending branches did not overlap. The frequency of collaterals of the TP afferents was less than that of the other types of afferents. The terminal arbors including the density of boutons of the pulpal afferents were less extensive than those of the other types of afferents. The average size of varicosities became smaller in the following subdivisions. Vp, Vo.r and Vo.dm for SA and TP afferents. The size of varicosities of the TP afferents was smaller and that of the FA afferents was larger than that of the SA afferents.(ABSTRACT TRUNCATED AT 400 WORDS)

Morphological and functional properties of trigeminal nucleus oralis neurons projecting to the trigeminal motor nucleus of the cat

Horseradish peroxidase (HRP) was injected into the somata located in the rostrodorsomedial part (Vo.r) of the trigeminal nucleus oralis; an axonal projection to the trigeminal motor nucleus (Vmo) was demonstrated in two Vo.r neurons. The two neurons differed in their morphological and functional properties. The first Vo.r neuron responded to stimulation of low-threshold mechanoreceptors and its stem axon gave off massive axon collaterals that issued terminal branches to the dorsolateral subdivision of Vmo, Vo.r, and the medial and lateral parts of the lower brainstem reticular formation. The second Vo.r neuron was activated by stimulation of the tooth pulp or lingual nerve at twice longer latency than that of the first neuron. This stem axon was divided into two main ascending and one descending branches, and one of the main ascending branches was further bifurcated into two branches. The main non-bifurcated ascending branch gave off 4 collaterals, two of which sent terminal branches into the dorsolateral subdivision of Vmo and others into the Vo.r and juxta-trigeminal regions. The somato-dendroarchitectonic differences were also described in the two Vo.r neurons stained.