Neuromechanisms of reciprocal interrelation between jaw-opening and jaw-closing muscles in the cat (author's transl)]

Neural controlling mechanisms between the digastric (jaw-opening) and masseter (jaw-closing) muscles were studied in the cat. High threshold afferent impulses from the anterior belly of the digastric muscle to masseteric montoneurons in the trigeminal motor nucleus induced an EPSP-IPSP sequence of potentials with long latency, and high threshold afferent impulses from the masseter muscle also exerted a similar effect on digastric motoneurons in the same nucleus innervating the anterior belly of the digastric muscle. These results suggest that reciprocal inhibition via Ia interneurons as observed between the flexor and extensor muscles in the spinal cord does not exist between the digastric and masseter muscles in the cat. However, the respective motoneurons innervating the masseter and digastric muscles receive inputs of early excitation-late inhibition via high threshold afferent nerve fibers from each antagonistic muscle. As such, since EPSPs preceding IPSPs are recognized, these high threshold afferent impulses may exert not only a reciprocal inhibitory effect, but also a synchronous excitatory or inhibitory effect on the antagonistic motoneurons.     

Supratrigeminal neurons mediate the shortest, disynaptic pathway from the central amygdaloid nucleus to the contralateral trigeminal motoneurons in the rat

Stimulation of the supratrigeminal area (STA) of the rat induced a monosynaptic EPSP in most mylohyoid-digastric motoneurons and a monosynaptic IPSP or EPSP in the majority of masseteric ones, contralaterally. Stimulation of the central amygdaloid nucleus induced the ipsilateral STA activity immediately followed by the contralateral mylohyoid nerve activities. The same amygdaloid stimulated excited 19 of 46 STA neurons, which were antidromically identified to project to the contralateral trigeminal motor nucleus. Nine of these were monosynaptically excited. The mean of the antidromic and monosynaptic latencies of these neurons explains the mean onset latencies of the amygdaloid influences on the contralateral trigeminal motoneurons. Therefore, the shortest crossing amygdalo-motoneuronal pathway is probably disynaptic and mediated by commissural STA neurons.     

Craniofacial sequelae of lesions to facial and trigeminal motor nuclei in growing rats

Unilateral electrolytic lesions were made in the left-side facial motor nucleus (FMNu) of six Sprague-Dawley rats at 35 days of age in order to correlate craniofacial sequelae with changed motoneuron function. Experimental and control rats were killed at 22, 32, 42, and 52 days postoperatively to provide muscle weight, brain histology, and dry skull preparations for analyses. Dissection, muscle weight, motoneuron count, and osteometric data revealed that lesion-side facial and masticatory muscles were affected by the lesions. Paired t-tests indicated that significant differences existed between weights of experimental lesion- and nonlesion-side anterior digastric, temporalis, masseteric complex, and medial pterygoid muscles, numbers of facial and trigeminal motoneurons, and several skeletal dimensions of the skull. Basi-cranial dimensions of experimental animals were least affected by the lesion, whereas zygomatic arch, dorsal facial region, and mandibular condyle dimensions were most affected. Statistical analyses also detected significant differences between experimental and control groups for several skeletal dimensions of the skull. Data indicated that damage to the trigeminal motor nucleus (TMNu) was secondary to the primary lesion in the FMNu. Motoneurons within the facial and trigeminal neuromuscular complexes (FNC and TNC) play an important role in craniofacial growth and development.     

Modulation of the masseteric reflex by gastric vagal afferents

Several investigations have shown that the vagal nerve can affect the reflex responses of the masticatory muscles acting at level either of trigeminal motoneurons or of the mesencephalic trigeminal nucleus (MTN). The present experiments have been devoted to establish the origin of the vagal afferent fibres involved in modulating the masseteric reflex. In particular, the gastric vagal afferents were taken into consideration and selective stimulations of such fibres were performed in rabbit. Conditioning electrical stimulation of truncus vagalis ventralis (TVV) reduced the excitability of the MTN cells as shown by a decrease of the antidromic response recorded from the semilunar ganglion and elicited by MTN single-shock electrical stimulation. Sympathetic and cardiovascular influences were not involved in these responses. Mechanical stimulation of gastric receptors, by means of gastric distension, clearly diminished the amplitude of twitch tension of masseteric reflex and inhibited the discharge frequency of proprioceptive MTN units. The effect was phasic and depended upon the velocity of distension. Thus the sensory volleys originating from rapid adapting receptors reach the brain stem through vagal afferents and by means of a polysynaptic connection inhibits the masseteric reflex at level of MTN cells.     

Doublecortin is expressed in trigeminal motoneurons that innervate the velar musculature of lampreys: considerations on the evolution and development of the trigeminal system

Studies in lampreys have revealed interesting aspects of the evolution of the trigeminal system and the jaw. In the present study, we found a marker that distinguishes subpopulations of trigeminal motoneurons innervating two different kinds of oropharyngeal muscles. Immunofluorescence with an antibody against doublecortin (DCX; a neuron-specific phosphoprotein) enabled identification of the trigeminal motoneurons that innervate the velar musculature of larval and recently transformed sea lampreys. DCX-immunoreactive (-ir) motoneurons were observed in the rostro-lateral part of the trigeminal motor nucleus of these animals, but not in lampreys 1 month or more after metamorphosis. Combined double DCX/tubulin and serotonin/tubulin immunofluorescence and tract-tracing experiments with neurobiotin (NB) were also performed in larvae for further characterization of this system. Rich innervation by DCX-ir fibers was observed on the muscle fibers of the velum but not on the upper lip or lower lip muscles, which were innervated by tubulin-ir/DCX-negative fibers. No double-labelled DCX-ir motoneurons were observed in experiments in which the tracer NB was applied to the upper lip. Innervation of velar muscles by serotonergic fibers is also reported. The present results indicate that development of the trigeminal motoneurons innervating the velum differs from that of the trigeminal motoneurons innervating the lips, which is probably related to the dramatic regression of the velum during metamorphosis. The absence of data on a similar subsystem in the trigeminal motor nucleus of gnathostomes suggests that they may be lamprey-specific motoneurons. These results provide support for the "heterotopic theory" of jaw evolution and are inconsistent with the theories of a velar origin for the gnathostome jaw.     

Synaptic potentials of digastric-muscle motoneurons

We studied the antidromic and synaptic potentials evoked from 32 digastric-muscle motoneurons by stimulation of the motor nerve to this muscle, different branches of the trigeminal nerve, and the mesencephalic trigeminal nucleus. Antidromic potentials appeared after 1.1 msec and lasted about 2.0 msec. Stimulation of the infraorbital, lingual, and inferior alveolar nerves led to development of excitatory postsynaptic potentials (EPSP) and action potentials in the motoneurons. The antidromically and synaptically evoked action potentials of the digastric-nerve motoneurons were characterized by weak after-effects. We were able to record EPSP and action potentials in two of the motoneurons investigated in response to stimulation of the mesencephalic trigeminal nucleus, the latent period being 1.3 msec. This indicates the existence of a polysynaptic connection between the mesencephalic-nucleus neurons and the digastric-muscle motoneurons. Eight digastric-muscle motoneurons exhibited inhibitory postsynaptic potentials (IPSP), which were evoked by activation of the afferent fibers of the antagonistic muscle (m. masseter). The data obtained indicate the presence of reciprocal relationships between the motoneurons of the antagonistic muscles that participate in the act of mastication.A. A. Bogomol'ts Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 3, No. 1, pp. 52–57, January–February, 1971.     

Morphological studies of the neuromuscular mechanism shifting from sucking to biting of mice

In order to give a neuroanatomical evidence to the mechanism of shifting from sucking to biting, we investigated in prenatal, newborn and postnatal mice whether there is a time difference in the neurogenesis of the neurons relative to sucking and biting or in the histogenesis of their peripheral effector organs by the HRP labeling technique and electron microscopy. The results obtained are as follows. (1) At birth the facial motoneurons exceed the trigeminal motoneurons in cell area and development. (2) After birth, the trigeminal motoneurons grow rapidly and outstrip the growth of the facial motoneurons at the age of 6 days. (3) Thereafter, the cell area of both neuron types continues to increase gradually. (4) The initial sign of the alpha motor end plates is found in the orbicularis oris muscle innervated by the facial nerve in 17-day-old fetuses, while that of the trigeminal nerve is delayed in the masseter muscle of 18-day-old fetuses. (5) The initial sign of the muscle spindle appears with the sensory terminals in the masseter muscle of 17-day-old fetuses and the fundamental structure of the muscle spindle is formed in 4-day-old youngs. (6) Myelination of the facial nerve begins in 3-day-old youngs, while that of the trigeminal nerve becomes apparent in 4- or 5-day-old youngs. From these bases, it is obvious that the facial nerve elements related to sucking are firstly developed at birth and that the differentiation of the trigeminal nerve elements related to biting is rapidly accelerated after birth.     

Tracing of lateral pterygoid muscle-related neurons in the trigeminal brainstem nuclei in the rat

Retrograde transport of fluorescent tracers (diamidino yellow and true blue) was used to study the arrangement of brainstem neurons innervating the lateral pterygoid muscle in the rat. The lateral pterygoid motoneurons were located in the dorsolateral (jaw-closing) part of the trigeminal motor nucleus with clear somatotopy in the caudal part of the nucleus. No muscle-related neurons were present in the mesencephalic trigeminal nucleus. Histological examination of serial sections of lateral pterygoid muscles confirms the notion that, at least in the rat, this muscle is devoid of muscle spindles.     

Arrangement of supramandibular and suprahyoid motoneurons in the rat; a fluorescent tracer study

The arrangement of the motoneurons innervating the supramandibular and suprahyoid muscles was studied in Wistar albino rats using two fluorescent tracers: nuclear yellow and true blue. All supramandibular motoneurons were found within the trigeminal motor nucleus; they appeared to be somatotopically arranged. The suprahyoid motoneurons were located in an accessory trigeminal-facial motor complex. No overlap of the motoneuron pools of the supramandibular and suprahyoid muscle group was observed. Only motoneurons ipsilateral to the treated muscles were labeled. It was shown that a one-to-one relationship always exists between motoneuron and muscle.     

Synaptic potentials of motoneurons of the masseter muscle

Postsynaptic potentials of 93 motoneurons of the masseter muscle evoked by stimulation of different branches of the trigeminal nerve were studied. Stimulation of the most excitable afferent fibers of the motor nerve of the masseter muscle evoked monosynaptic EPSPs with a latent period of 1.2–2.0 msec, changing into action potentials when the strength of stimulation was increased. A further increase in the strength of stimulation produced an antidromic action potential in the motoneurons with a latent period of 0.9 msec. In some motoneurons polysynaptic EPSPs and action potentials developed following stimulation of the motor nerve to the masseter muscle. The ascending phase of synaptic and antidromic action potentials was subdivided into IS and SD components, while the descending phase ended with definite depolarization and hyperpolarization after-potentials. Stimulation of cutaneous branches of the trigeminal nerve, and also of the motor nerve of the antagonist muscle (digastric) evoked IPSPs with a latent period of 2.7–3.5 msec in motoneurons of the masseter muscle. These results indicate the existence of functional connections between motoneurons of the masseter muscle and its proprioceptive afferent fibers, and also with proprioceptive afferent fibers of the antagonist muscle and cutaneous afferent fibers.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 1, No. 3, pp. 262–268, November–December, 1969.     

Localization and morphometric analysis of masticatory muscle afferent neurons in the nucleus of the mesencephalic root of the trigeminal nerve in the cat

Injections of horseradish peroxidase (HRP) were made into the ipsilateral temporal muscle and contralateral masseter muscle of 10 cats in order to identify and characterize neurons in the nucleus of the mesencephalic root of the trigeminal nerve that innervate muscle receptors in the orofacial periphery. Neurons labelled by HRP injections and unlabelled cells from 5 control cats were measured with a computer-based image analyzer, and their position was mapped on a stereotaxic graph. Cells that innervate the masseter and temporal muscles were identified throughout the rostrocaudal extent of the nucleus. There was no indication of a somatotopic pattern nor of a specific segregation within the nucleus for cells innervating muscle receptors. The nucleus contained small, rounded unipolar neurons located primarily in the dorsal border of the periaqueductal gray (PAG) matter in the rostral part of the nucleus and larger oval unipolar neurons which were scattered throughout the nucleus, but were predominant in the pontine portion of the nucleus. HRP injections labelled both large and small cells, as well as occasional multipolar cells. The last-mentioned tended to be located in the lateral margins of the PAG. The mean geometric values obtained for the control group were: area 552.7 microns2 perimeter 110.3 microns; maximum diameter 36.0 microns. and diameter of an equivalent circle 26.1 microns. The mean values of the labelled neurons were: area 606.6 microns2; perimeter 100.1 microns; maximum diameter 36.0 microns, and diameter of an equivalent circle 27.2 microns.     

Functional properties of interneurons of the masticatory reflex

Interneurons of the supratrigeminal nucleus, transmitting effects from the sensory and motor branches of the trigeminal nerve to motoneurons of the muscles of mastication were investigated. Two groups of interneurons with different functional connections were found. The first group (A) contains neurons excited during stimulation of the sensory branches and the motor nerve to the digastric muscle (A₁), neurons excited during stimulation of sensory branches and high-threshold afferents of the motor nerve to the masseter muscle (A₂), and neurons excited only by low-threshold afferents of the motor nerve to the masseter muscle (A₃). Neurons of the second group (B) were activated only by sensory fibers of the trigeminal nerve. It is postulated that interneurons of group A transmit inhibitory effects to motoneurons of antagonist muscles of the lower jaw. Group B interneurons participate in the transmission of excitatory influences to motoneurons of the digastric muscle.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 4, No. 2, pp. 150–157, March–April, 1972.     

Positive feedback in a brainstem tactile sensorimotor loop

The trigeminal loop in the brainstem comprises the innermost level of sensorimotor feedback in the rat vibrissa system. Anatomy suggests that this loop relays tactile information from the vibrissae to the motoneurons that control vibrissa movement. We demonstrate, using in vitro and in vivo recordings, that the trigeminal loop consists of excitatory pathways from vibrissa sensory inputs to vibrissa motoneurons in the facial nucleus. We further show that the trigeminal loop implements a rapidly depressing reflex that provides positive sensory feedback to the vibrissa musculature during simulated whisking and contact. On the basis of these findings, we propose that the trigeminal loop provides an enhancement of vibrissa muscle tone upon contact during active touch.     

Morphological alteration in oro-facial CGRP containing motoneurons due to congenital thyroid hypofunction

Under congenital thyroid hypofunction, the oro-facial large and small calcitonin gene-related peptide (CGRP) immunoreactive motoneurons were classified into strong, moderate, weak and negative intensity in offspring weaned rats. While 50% of neurons in the trigeminal motor nucleus (Mo5) were of the large type, this value dropped to 30% in hypothyroid pups. Hypothyroid trigeminal accessory nucleus (Mo5-AC) contained 10% large motoneurons versus about 45% in normal pups. Normal facial nucleus (Mo7) had 20% large motoneurons in contrast with 10% in hypothyroid pups. These values are significant in comparison with the normal pattern of oro-facial CGRP positive immunoreactive motoneurons as well as those devoid of immunostaining.     

Amygdaloid-induced jaw opening and facilitation or inhibition of the trigeminal motoneurons in the rat

1. Repetitive stimulation of the rat'se central amygdaloid (CAm) nucleus induced rhythmic masticatory jaw movements or continuous jaw opening. Both types of jaw movements were accompanied by coincidental activities of the mylohyoid (Myl) nerve. 2. The effects of CAm stimulation were examined on activities of bilateral Myl and masseteric (Mass) nerves or their motoneurons (Myl-Dig and Mass, respectively). 3. CAm stimulation induced contralaterally dominant facilitation of the Myl nerve activity as well as Myl-Dig motoneurons. These facilitatory effects were caused by EPSPs seen in Myl-Dig motoneurons. 4. One third of the Mass motoneurons were inhibited or hyperpolarized by contralateral CAm stimulation, while a few were facilitated and the majority unaffected.     

Membrane electrical properties of motoneurons innervating the masseter muscles in rats

Membrane potentials and action potentials evoked by antidromic and direct stimulation were investigated in motoneurons of the trigeminal nucleus in rats innervating the masseter muscle. This motor nucleus was shown to contain cell populations with high and low membrane potentials. The responses of cells of the first group had shorter latent periods of their antidromic action potentials, a longer spike duration, and a lower amplitude and shorter duration of after-hyperpolarization than responses of cells of the second group, and the input resistance of their membrane also is lower. The bimodal character of distribution of electrophysiological parameters of motoneurons in the trigeminal nucleus indicates that "fast" and "slow" fibers of the masseter muscles may be innervated by different types of nerve cells.N. A. Semashko Moscow Medical Stomatological Institute. Translated from Neirofiziologiya, Vol. 13, No. 3, pp. 270–274, May–June, 1981.     

Masseteric Nerve Injury Increases Expression of Brain-Derived Neurotrophic Factor in Microglia Within the Rat Mesencephalic Trigeminal Tract Nucleus

The distribution of brain-derived neurotrophic factor was examined in the rat mesencephalic trigeminal tract nucleus after transection and crush of the masseteric nerve. In the intact mesencephalic trigeminal tract nucleus, brain-derived neurotrophic factor was detected in small cells with fine processes. These cells and processes were occasionally located adjacent to tyrosine kinase B receptor-immunoreactive sensory neurons. The transection and crush of the masseteric nerve increased expression of brain-derived neurotrophic factor in the nucleus. The number and size of brain-derived neurotrophic factor-immunoreactive cells and processes were dramatically elevated by the nerve injury. As a result, the density of brain-derived neurotrophic factor-immunoreactive profiles in the mesencephalic trigeminal tract nucleus at 7 days after the injury was significantly higher compared with the intact nucleus. Double immunofluorescence method also revealed that brain-derived neurotrophic factor-immunoreactive cells were mostly immunoreactive for OX-42 but not glial fibrillary acidic protein. In addition, the retrograde tracing method demonstrated that brain-derived neurotrophic factor-immunoreactive cells and processes surrounded retrogradely labeled neurons which showed tyrosine kinase B receptor-immunoreactivity. These findings indicate that the nerve injury increases expression of brain-derived neurotrophic factor in microglia within the mesencephalic trigeminal tract nucleus. The glial neurotrophic factor may be associated with axonal regeneration of the injured primary proprioceptor in the trigeminal nervous system.     

Corticofugal influences on the motoneurons of the trigeminal nucleus

We studied the postsynaptic potentials evoked from 76 trigeminal motoneurons by stimulation of the motor (MI) and somatosensory (SI) cortex in the ipsilateral and contralateral hemispheres of the cat. Stimulation of these cortical regions evoked primarily inhibitory postsynaptic potentials (PSP) in the motoneuron of the masseter muscle, but we also observed excitatory PSP and mixed reactions of the EPSP/IPSP type. The average IPSP latent period for the motoneurons of the masseter on stimulation of the ipsilateral cortex was 6.1±0.3 msec, while that on stimulation of the contralateral cortex was 5.2±0.4 msec; the corresponding figures for the EPSP were 7.6±0.5 and 4.5±0.3 msec respectively. Corticofugal impulses evoked only EPSP and action potentials in the motoneurons of the digastric muscle (m. digastricus). The latent period of the EPSP was 7.6 msec when evoked by afferent impulses from the ipsilateral cortex and 5.4 msec when evoked by pulses from the contralateral cortex. The duration of the PSP ranged from 25 to 30 msec. Postsynaptic potentials developed in the motoneurons studied when the cortex was stimulated with a single stimulus. An increase in the number of stimuli in the series led to a rise in the PSP amplitude and a reduction in the latent periods. When the cortex was stimulated with a series of pulses (lasting 1.0 msec), the IPSP were prolonged by appearance of a late slow component. We have hypothesized that activation of the trigeminal motoneurons by corticofugal impulsation is effected through a polysynaptic pathway; each functional group of motoneurons is activated in the same manner by the ipsilateral and contralateral cortex. The excitation of the digastric motoneurons and inhibition of the masseter motoneurons indicates reciprocal cortical control of their activity.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 3, No. 5, pp. 512–519, September–October, 1971.     

Role of GABA<Subscript>B</Subscript> receptor in the regulation of excitatory synaptic transmission in trigeminal motoneurons

The aim of the present study was to determine if excitatory synaptic transmission onto trigeminal motoneurons is subject to a presynaptic modulation by gamma-aminobutyric acid (GABA) via GABA(B) receptor in this system. Whole cell recordings were made from trigeminal motoneurons in longitudinal brain stem slices taken from 8-day-old rats. Monosynaptic excitatory postsynaptic potential (EPSP) activity was evoked by placing bipolar stainless steel electrodes dorsal-caudal to the trigeminal motor nucleus. Bath application of the GABA(B) receptor agonist, baclofen, produced a marked reduction in the mean amplitude and variance of evoked EPSPs and also increased the portion of transmission failures. It also produced a decrease in the frequency, but not in the mean amplitude, of spontaneous miniature EPSPs. Bath application of GABA(B) receptor antagonists 6-hydroxy-saclofen and CGP35348 increased both the amplitude and frequency of miniature EPSP activity. Taken together the above results suggest that the excitatory synaptic inputs onto trigeminal motoneurons are controlled by tonic presynaptic modulation by GABA(B) receptor.