Excitatory and inhibitory effects of lingual nerve stimulation on reflexes controlling the activity of masseteric motoneurons

doi:10.1016/0006-8993(72)90787-1

Brain Research

Volume 39, Issue 1, 14 April 1972, Pages 95-108

https://doi.org/10.1016/0006-8993(72)90787-1 Get rights and content

Abstract

The masseteric reflex was suppressed for 200–400 msec following a single shock stimulus to low threshold fibers in either the ipsilateral or contralateral lingual nerve of decerebrate cats. There were two phases of suppression; the maximum reduction in the amplitude of the reflex occurred 5–10 msec after the stimulus in the first phase, and approximately 40 msec after the stimulus in the second phase. Between these two phases of suppression was a recovery period characterized by an increase in reflex amplitude.

Following midline section of the brain stem between the trigeminal motor nuclei the first phase of suppression of the masseteric reflex induced by contralateral lingual nerve stimulation was completely blocked. It was replaced by a facilitation of the reflex which occurred from 4 to 16 msec after the contralateral stimulus. The second phase of suppression was not effected by the section.

The intravenous injection of picrotoxin did not effect the first phase of suppression but significantly reduced the degree of suppression attained in the second phase.

Stimulation of the contralateral lingual nerve induced primary afferent depolarization (PAD) in ipsilateral lingual nerve terminals. The same contralateral stimulus also blocked the first phase of suppression of the masseteric reflex induced by ipsilateral lingual nerve stimulation. The time course of the disinhibitory effect was similar to that of the PAD, and the proposal was made that depolarization of the ipsilateral terminals was responsible for the disinhibition.

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Symmetrical motor output is the rule in the masticatory system. We examined morphologically how this functional symmetry might be reflected in the organization of premotor neurons that could mediate excitation of jaw-opener motoneurons. Premotor neurons projecting bilaterally to jaw-opener motoneurons by way of axon collaterals were identified by retrograde dual-labeling with cholera toxin B-conjugated fluorescein isothiocyanate (CTb-FITC) and tetramethylrhodamine (TMR). In each cat, CTb-FITC and TMR were injected into the digastric motoneuron pools, respectively, on the left and right sides. In three animals, 69–147 neurons were labeled with both tracers, comprising ∼44% of all retrogradely labeled cells. Double-labeled cells were located bilaterally in the trigeminal oral nucleus (Vo) and the adjacent reticular formation (RF), the former containing a larger number of cells. Neurons labeled with only one tracer were also distributed bilaterally in the Vo and RF. The results indicated that the bilaterally projecting premoter neurons identified mainly in the Vo and RF represent neuronal substrates for the symmetry that characterizes most jaw movements.
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The aim of this study was to determine the effect of unilateral acute inflammation of craniofacial deep tissues on the ipsilateral and contralateral jaw-opening reflex (JOR). The effects of mustard oil (MO), injected into the temporomandibular joint region, were tested on the JOR recorded in the digastric muscle and evoked by low-intensity electrical stimulation of the ipsilateral and contralateral inferior alveolar nerve in anesthetized rats. The MO injection induced a long-lasting suppression of the amplitude of both ipsilaterally and contralaterally evoked JOR, although the latency and duration of the JOR were unaffected. The suppressive effect was more prominent for the contralaterally evoked JOR, and observed even when background activity in the digastric muscle was increased by the MO injection. The results indicate that changes in the JOR amplitude following MO injection do not simply reflect alterations in motoneuronal excitability, and suggest that inflammation of deep craniofacial tissues modulates low-threshold sensory transmission to the motoneurons.
Modulation of an inhibitory reflex in single motor units in human masseter by tonic painful stimulation
1999, Pain
Perioral electrical stimuli cause inhibitory reflex responses in single motor-units (SMU) and surface electromyographic (EMG) recordings from voluntary contracted human jaw-closing muscles. Tonic experimental masseter pain has recently been shown to reduce the inhibitory reflex response in surface EMG recordings but the effect on SMU activity has not been described. In this study, motor-unit action potentials were recorded with wire electrodes inserted into the left masseter in eleven subjects. The subjects kept the SMU firing rate around 10 Hz by feedback. Ninety-nine electrical stimuli were applied sequentially to the left mental nerve with increasing stimulus delays in steps of 1 ms after the preceding motor unit action potential. The inhibitory reflex in SMU was recorded before, during and after infusion of hypertonic saline (5%) into the ipsilateral masseter muscle. Spike train data were used to calculate (1) the mean pre- and post-stimulus inter-spike-intervals (ISI) in all of the 99 trials, (2) cumulative changes in firing probability, and (3) estimation of the compound inhibitory post-synaptic potential (IPSP) in the masseter motoneuron. Tonic masseter pain did not change pre-stimulus SMU firing characteristics but the mean ISI for the first post-stimulus discharge (158.2±9.2 ms) was significantly decreased compared to the pre-pain (175.8±11.3 ms, P<0.05) and post-pain conditions (172.6±11.6 ms, P<0.05). The post-stimulus firing probability was significantly increased and the relative amplitude of the estimated IPSP significantly decreased during tonic masseter pain compared to pre-pain and post-pain conditions. In conclusion, this study indicates that tonic masseter pain has a net excitatory effect on the inhibitory jaw-reflexes, which could be mediated by presynaptic mechanisms on the involved motoneurons.
Glycine-immunoreactive terminals in the rat trigeminal motor nucleus: Light- and electron-microscopic analysis of their relationships with motoneurones and with GABA-immunoreactive terminals
1997, Brain Research
Post-embedding immunolabelling methods were applied to semi-thin and ultrathin resin sections to examine the relationships between glycine- and γ-aminobutyric acid (GABA)-immunoreactive terminals on trigeminal motoneurones, which were identified by the retrograde transport of horseradish peroxidase injected into the jaw-closer muscles. Serial sections were cut through boutons and alternate sections were incubated with antibodies to glycine and GABA. Light-microscopic analysis of semi-thin sections revealed a similar pattern of glycine and GABA-immunoreactive boutons along the motoneurone soma and proximal dendrites, and of immunoreactive cell bodies in the parvocellular reticular and peritrigeminal areas surrounding the motor nucleus. Immunoreactive synaptic terminals on motoneurones were identified on serial ultrathin sections at electron-microscopic level using a quantitative immunogold method. Three populations of immunolabelled boutons were recognized: boutons immunoreactive for glycine alone (32%), boutons immunoreactive for GABA alone (22%), and boutons showing co-existence of glycine and GABA immunoreactivities (46%). Terminals which were immunoreactive for glycine only contained a higher proportion of flattened synaptic vesicles than those which were immunoreactive for GABA only, which contained predominantly spherical vesicles. Terminals which exhibited both immunoreactivities contained a mixture of vesicle types. All three classes of terminal formed axo-dendritic and axo-somatic contacts onto retrogradely labelled motoneurones. A relatively high proportion (25%)of boutons that were immunoreactive for both transmitters formed synapses on somatic spines. However, only GABA-immunoreactive boutons formed the presynaptic elements at axo-axonic contacts: none of these were found to contain glycine immunoreactivity. These data provide ultrastructural evidence for the role of glycine and GABA as inhibitory neurotransmitters at synapses onto jaw-closer motoneurones, but suggest that presynaptic control of transmission at excitatory (glutamatergic) synapses on motoneurones involves GABAergic, but not glycinergic inhibition.
Supra- and juxtatrigeminal inhibitory premotor neurons with bifurcating axons projecting to masseter motoneurons on both sides
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Inhibitory neurons participating in the bilateral disynaptic inhibition of jaw-closing motoneurons by stimulation of unilateral trigeminal sensory branches were searched for in the reticular formation around the trigeminal motor nucleus in cats anaesthetized with pentobarbital. Extracellular recordings were made from neurons which responded orthodromically after a monosynaptic latency to single shock stimulation of the ipsilateral infraorbital and/or inferior alveolar nerves. Direct inhibitory connection with contralateral masseter motoneurons was demonstrated in reticular neurons by the spike-triggered averaging technique, i.e., by averaging the intracellular potentials of a contralateral masseter motoneuron with respect to spontaneously occurring spikes of a reticular interneuron. By intraaxonal injection of neurobiotin, electrophysiologically identified inhibitory premotor reticular neurons were found to project to and to terminate in the trigeminal motor nuclei on both sides. Termination in the contralateral motor nucleus was demonstrated for four neurons that showed the peripheral input pattern stated above. The results provide hard evidence for contralaterally projecting interneurons in the reticular formation, participating in peripherally evoked disynaptic inhibition of masseter motoneurons on the contralateral side. Given the previously reported findings that the supratrigeminal region contains neurons which project to the ipsilateral motor nucleus and mediate disynaptic inhibition of masseter motoneurons, it is suggested that the supratrigeminal region contains bilaterally projecting interneurons, mediating peripherally evoked disynaptic inhibition of masseter motoneurons on both sides.
Masseteric facilitation induced by electrical stimulation of rat orofacial tissues
1992, Archives of Oral Biology
The effects of a conditioning electrical shock applied to the periodontium of the lower incisor or the glabrous area of the lower lip on the jaw-closing reflex in the anaesthetized, non-paralysed rat were studied. The masseteric reflex was triggered by stimulation of the mesencephalic nucleus as a test shock and was recorded from the masseter muscle. There was facilitation of the jaw-jerk reflex, which culminated at an interval of 10–15ms between the conditioning and the test shocks. This facilitation was not suppressed by digastric excision or by blocking a possible rebound closing reflex evoked by jaw opening. No inhibitory influence was observed. This facilitatory effects relies on an A alpha input and on cell bodies making up the mesencephalic nucleus. The direct excitatory electrical events observed in the masseter muscle after periodontal or labial stimulation proved to be due to the diffusion of the bioelectrical activity generated in the neighbouring jaw-opening muscles.

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Excitatory and inhibitory effects of lingual nerve stimulation on reflexes controlling the activity of masseteric motoneurons

Abstract

J. prosth. Dent.

Brain Research

Brain Research

Brain Research

Exp. Neurol.

Le réflexe linguomaxillaire chez le cheval

C. R. Soc. Biol. (Paris)

Histologie du Système Nerveux de l'Homme et des Vertébrés

Inhibition of a monosynaptic reflex by electrical stimulation of the basal forebrain or the orbital gyrus in the cat

Experientia (Basel)

Pharmacological studies on presynaptic inhibition

J. Physiol. (Lond.)

Disinhibition in the trigeminal system

Anat. Rec.

Lingually induced inhibition of masseteric motoneurones

Experientia (Basel)

Reflex jaw opening in response to stimulation of periodontal mechanoreceptors in the cat

Arch. oral Biol.

The central pathway for the jaw-jerk

Amer. J. Physiol.