Effects of afferent firing frequency on the amplitude of the monosynaptic EPSP elicited by trigeminal spindle afferents on trigeminal motoneurones

We have examined the effect of changes in afferent firing frequency on the monosynaptic EPSP elicited by trigeminal muscle spindle afferents in elevator motoneurones, using both paired pulse and repetitive activation of the masseter nerve. Both modes of stimulation resulted in significant facilitation of EPSP amplitude over intervals of 5–19 ms, but no significant change in EPSP amplitude at either longer or shorter intervals. The facilitation obtained stands in contrast to the predominant depression of EPSP amplitude reported in hindlimb motoneurones following stimulation at decreasing intervals.     

Focal blockade of single unit synaptic transmission by iontophoresis of antagonists.

We have assessed the use of iontophoresis for investigating the pharmacology of synaptic transmission from individual presynaptic neurones in-vivo, by modifying extracellular focal synaptic potentials (FSPs) recorded by spike-triggered averaging. FSPs from two types of excitatory neurone (muscle spindle primary afferents and expiratory bulbospinal neurones) and from one inhibitory interneurone were studied in the thoracic ventral horn of anaesthetized cats. The antagonist of excitatory amino acids at non-NMDA receptors, DNQX, blocked the FSPs from the first two, as did bicuculline for the third. Thus the FSPs were generated by excitatory amino acids acting via non-NMDA receptors and GABA, respectively. The postsynaptic neurones were probably motoneurones. Merits and limitations of the method are discussed.     

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.     

Physiologic and morphologic properties of motoneurons and spindle afferents innervating the temporal muscle in the cat

Little is known about physiology and morphology of motoneurons and spindle afferents innervating the temporalis and on synaptic connections made between the two. The present study was aimed at investigating the above issues at the light microscopic level by using the intracellular recording and horseradish peroxidase or biotinamide labeling techniques and by the use of succinylcholine (SCh) for the classification of spindle afferents in the cat. Temporalis motoneurons had dendritic trees that ranged from a spherical form to an egg-shaped form. The shape deformation was more prominent for the dendritic trees made by motoneurons located closer to the nuclear border. No axon collaterals of the motoneurons were detected. On the basis of the values for the dynamic index after SCh infusion, temporalis spindle afferents were classified into two populations: presumptive groups Ia and II. The spindle afferents terminated mainly in the supratrigeminal nucleus (Vsup), region h, and the dorsolateral subdivision (Vmo.dl) of the trigeminal motor nucleus (Vmo). The proportion of group Ia afferent terminals was lower in the Vsup than that of group II afferents. In the Vmo.dl, the proportion of group Ia afferent terminals was nearly even throughout the nucleus, but that of group II afferent terminals increased in the more outlying regions. The proportion of terminal distribution in the central region of Vmo.dl was higher for group Ia than group II. The frequency of contacts (presumptive synapses) made by a single spindle afferent on a motoneuron was higher for group Ia than group II. The present study provided evidence that the central organization of spindle afferent neurons is different between groups Ia and II.     

Distribution of the human jaw stretch reflex response elicited by percutaneous, localized stretch of jaw-closing muscles

In the present study homonymous and heteronymous projections of muscle spindle afferent fibers in the human jaw-closing system were investigated. Stretch reflex responses were elicited with percutaneous displacement stimuli applied to the belly of the anterior superficial divisions of temporalis and masseter muscles. The distribution of reflex responses in jaw-closing muscles was assessed. Reflex responses to this stimulus were observed in all jaw-closing muscles ipsilateral to the stimulated muscle, suggesting that the projection of spindle afferent fibers to jaw-closing muscles in humans is diffuse. Comparisons of homonymous and heteronymous reflex response amplitudes indicated that homonymous response amplitudes tended to be larger. However, the relative strength of heteronymous inputs to masseter motoneurons appeared to be stronger than those to temporalis motoneurons.     

Presynaptic inhibition of muscle spindle and tendon organ afferents in the mammalian spinal cord

More than 30 years ago, Frank and Fuortes proposed that the synaptic effectiveness of muscle spindle afferents associated with spinal motoneurones could be diminished by the activation of nerves from flexor muscles. Since that time, research has focused on disclosing the mode of operation and the spinal pathways involved in this presynaptic inhibitory control. Initially, it was assumed that the same last-order interneurones mediated presynaptic inhibition of both muscle spindle and tendon organ afferent fibres. More recent evidence indicates that the synaptic effectiveness of these two groups of afferents is controlled by separate sets of GABAergic interneurones synapsing directly with the intraspinal terminals of the afferent fibres. This unique arrangement allows for selective control of the information on muscle length or muscle tension, despite the convergence of muscle spindle and tendon organ afferents on second-order interneurones.     

Soma size and oxidative enzyme activity of motoneurons supplying the fast twitch and slow twitch muscles in the rat

The relationship between soma size and oxidative enzyme activity of motoneurones supplying the fast twitch muscle and the slow twitch muscle was examined. Horseradish peroxidase was injected into the extensor digitorum longus (fast twitch) muscle and the soleus (slow twitch) muscle to retrogradely label corresponding motoneurones of the rat spinal cord. There was a negative relation between some size and oxidative enzyme activity of motoneurones in a particular neurone pool. The alpha motoneurones supplying the slow twitch muscle had higher oxidative enzyme activities than identical size motoneurones supplying the fast twitch muscle. The present results suggest that there is a difference between oxidative capacities of fast twitch and slow twitch neurone pools.     

Central distribution of synaptic contacts of primary and secondary jaw muscle spindle afferents in the trigeminal motor nucleus of the cat

Little is known about the differences of the terminations of group Ia and group II afferents within the brainstem or spinal cord. The present study was performed to classify cat jaw muscle spindle afferents by the use of succinylcholine (SCh) and to examine the morphological characteristics of the physiologically classified afferents at the light and electron microscopic levels through the use of the intra-axonal horseradish peroxidase (HRP) injection technique. The effects of SCh on stretch responses of 119 jaw muscle spindle afferents from the masseter were examined. The SCh converted the single skew distribution of the values for dynamic index (DI) into a bimodal one. Fifty-eight and 61 afferents were classified as group Ia and group II afferents, respectively. The central projections of 17 intra-axonally stained afferents (10 group Ia and 7 group II afferents) were examined. The spindle afferents terminated mainly in the supratrigeminal nucleus (Vsup), region h, and the dorsolateral subdivision of trigeminal motor nucleus (Vmo.dl) but differed in the pattern of projections of group Ia and group II afferents. The proportion of group Ia afferent terminals was higher in Vmo.dl but lower in Vsup than that of group II afferents. In Vmo.dl, the proportion of group Ia afferent terminals was higher in the central region but lower in the more outer regions than that of group II afferents. The ultrastructure of serially sectioned afferent boutons (63 group Ia and 72 group II boutons) also was examined. The boutons from the two groups were distributed widely from the soma to small-diameter dendrites, but the frequency of synaptic contacts on proximal dendrites was higher in group Ia than group II afferents. The present study provides evidence that the two groups of jaw muscle spindle afferents differ in their central projection and the spatial distribution of their synaptic contacts on Vmo.dl neurons. J. Comp. Neurol. 391:50–63, 1998. © 1998 Wiley-Liss, Inc.     

Light microscopic observations of the contacts made between two spindle afferent types and α-motoneurons in the cat trigeminal motor nucleus

Previous studies indicate that cat jaw-muscle spindle afferents can be divided into two types (type I and II) on the basis of their axonal trajectories. The present study examined the relationship between spindle afferent fibers and their target masseter α-motoneurons in the cat by using the intracellular horseradish peroxidase (HRP) injection technique, and provided several new findings on the synaptic organization generated between the two. Five type I afferent fiber-motoneuron pairs and nine type II afferent-motoneuron pairs were well stained with HRP. The following conclusions were drawn: 1) A motoneuron received contacts from only one collateral of any given spindle afferent. 2) The number of contacts made between an afferent and a motoneuron ranged from one to three. 3) The contacts made by a spindle afferent were on the same dendrite or dendrites branching from the same primary dendrite. 4) The vast majority of the contacts made by an afferent on a motoneuron were distributed in the dendritic tree within 600 μm from the soma, i.e., in the proximal three fourths of the dendritic tree. The differences observed between the two afferent types were as follows. First, type II afferent terminals made contacts on more distal dendrites of the motoneurons than did type I afferent terminals. Second, the contacts made between a type I afferent and a motoneuron were clustered together, but those made between a type II afferent and a motoneuron were widely dispersed. The present results provided the general rules of synaptic contacts between the spindle afferents and masseter α-motoneurons, and demonstrated that the spatial distribution of synaptic contacts on the dendritic tree was different between type I and type II afferents. © 1996 Wiley-Liss, Inc.     

Pure trigeminal motor neuropathy presenting with temporo-mandibular joint dysfunction in a patient with HIV and HCV infections

Pure trigeminal motor neuropathy (PTMN) is a rarely described condition. We report the case of a 41-year-old woman infected with the human immunodeficiency virus (HIV1) and hepatitis C virus who presented with weakness of left temporalis and masseter muscles and painful left temporomandibular joint dysfunction (TMD) a few months after cerebral toxoplasmosis revealing acquired immunodeficiency syndrome (AIDS). Magnetic resonance imaging revealed severe wasting and fat replacement of the left temporalis, pterygoid and masseter muscles and showed neither abnormalities in the left motor nucleus of the trigeminal nerve nor compression of the left trigeminal nerve. Electromyographic examination gave evidence of denervation in the left temporalis, masseter and pterygoid muscles and blink reflex studies were normal, confirming the diagnosis of PTMN which was probably secondary to HIV and HCV co-infection.     

Organisation of common inputs to motoneuron pools of human masticatory muscles.

OBJECTIVE: To determine the pattern of organization of common inputs to the motoneuron pools of individual muscles in the masticatory system. METHODS: Six subjects bit on a rubber-coated wooden splint placed between the upper and lower incisor teeth. We recorded the surface electromyogram (EMG) of co-contracting masseter, temporalis and digastric muscles bilaterally during isometric jaw closing at 5%, 10%, 20% and 40% of maximal voluntary masseter EMG. RESULTS: The cross-correlograms of the EMGs of homologous muscle pairs indicate that there are common synaptic inputs to the motoneuron pools of the left and right masseter, and left and right digastric muscles, but not to left and right temporalis. The amplitude of the central peak in masseter and digastric correlograms increased with bite force. When the activity of ipsilateral muscle pairs was cross-correlated, central peaks were prominent for masseter-digastric and masseter-temporalis muscle pairs, and the peak amplitudes increased significantly with bite force. In contrast, no significant central peak was observed for temporalis-digastric muscle pairs at any level of voluntary biting. CONCLUSIONS: We conclude that there is synchronous modulation of input bilaterally to the masseter muscles and to the digastric muscles but not to the temporalis muscles. There is synchronous modulation of input to ipsilateral masseter-digastric and masseter-temporalis muscle pairs but not to temporalis and digastric muscles. SIGNIFICANCE: The extent of common input to motoneuron pools of muscles acting around a common joint varies for different muscle pairs, and is not simply a function of whether the muscles of the pair are synergists or antagonists.     

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

The objective of this study was to examine anatomically the distribution of afferent neurones in the mesencephalic nucleus of the fifth nerve (Mes V). HRP was applied, in separate experiments, to the inferior alveolar, infraorbital, and masseter nerves, and injected into the masseter muscle and periodontal ligament. Following application of HRP to the masseter muscle and masseter nerve, labelled cells were found in the ipsilateral motor nucleus of the fifth nerve and in the ipsilateral Mes V. Labelled cells in Mes V, identified as belonging to proprioceptor afferents from jaw-closing muscles, were distributed throughout the full extent of the nucleus. Following application of HRP to the inferior alveolar nerve, infraorbital nerve, and periodontal ligament, labelled cells were found in the ipsilateral trigeminal ganglion and Mes V, and the latter identified as belonging to periodontal receptor afferents. In contrast to the distribution of spindle afferent somata, they were restricted to the caudal region of Mes V. The differential distribution of afferent neurones within Mes V demonstrated in this study confirms previous electrophysiological findings, and its significance is considered.     

Effects of extensor and flexor group I afferent volleys on the excitability of individual soleus motoneurones in man

The contour of the postsynaptic potential (PSP) produced in a neurone by an afferent volley can be derived from the contour of the post-stimulus time histogram (PSTH) of that neurone when it is discharging rhythmically. In the present study the PSTH of the firing of individual soleus motor units after stimulation of the popliteal or peroneal nerve was used to explore the effects of extensor and flexor group I afferent volleys on the excitability of single soleus motoneurones in man. Extensor group I volleys resulted in an early peak of increased impulse density in the PSTH of 75% of soleus motoneurones. The latency suggests an analogy with the Ia EPSP. The mean duration of the peak of increased impulse density, equivalent to the rise time of the EPSP, was 3.6 ms. Flexor group I volleys result in a period of reduced impulse density in the PSTH of five out of nine soleus motoneurones. The latency suggests an analogy with the Ia IPSP. We conclude that this method could be used to explore the afferent connections to single motoneurones in man and to derive some of the characteristics of the postsynaptic potentials from a variety of afferent nerve fibres in single human motoneurones.     

Surface EMG recording of heteronymous reflex excitation of semitendinosus motoneurones by group II afferents.

OBJECTIVE: A potent stretch reflex originates in muscle spindle secondary endings and is mediated by group II muscle afferents. Electrical stimulation of peripheral nerve could also induce group II facilitation, as found in single motor unit recordings for various nerve-muscle combinations in man. The aim of the present investigation was to use surface electromyogram (EMG) to record and to quantify heteronymous excitation of semitendinosus (ST) motoneurones by group II afferents of the tibial nerve. METHODS: This study included 20 healthy subjects. The conditioning stimulation of the tibial nerve was delivered at the popliteal fossa at two intensity levels and for two levels of ST contraction. EMG activity was recorded by surface electrodes placed over the ST muscle, and the averaged and rectified ST EMG signal was analyzed. RESULTS: We observed 4 periods of interest: a first period of prestimulus background EMG activity; a second period of early reinforcement of ST EMG activity starting 30 ms poststimulus and lasting for 35-45 ms; a third period of relative inhibition of ST contraction; a fourth period of late reinforcement of poststimulus ST EMG activity. CONCLUSIONS: We hypothesized that the early period of facilitation was mainly related to heteronymous excitation of ST motoneurones by group II afferents on the basis of the following observations: (i) the amount of facilitation increased for a high stimulus intensity level, which was suitable for group II recruitment; (ii) the onset latency of this facilitation was consistent with the theoretically calculated latency of a group II-mediated reflex. SIGNIFICANCE: Surface EMG recording offers various advantages compared to single motor unit recording to study group II facilitation in the ST muscle. This technique could be applied in the future to confirm that heteronymous reflex excitation by group II afferents is enhanced in spastics and plays an important role in the development of lower limb spasticity.     

Synaptic connections to individual tibialis anterior motoneurones in man.

The characteristics of post-synaptic potentials in a single human motoneurone can be derived from the profiles of post-stimulus time histograms (PSTH) of that neurone when it is firing rhythmically. We have used this method to explore the synaptic connections to individual tibialis anterior motoneurones in man. Agonist group 1 volleys produced short latency excitation of 85% of tibialis anterior motoneurones probably representing the 1a EPSP. Excitation, at a latency of 70 ms, is attributed to a long loop reflex. Antagonist group 1 volleys produced short latency inhibition of 65% of tibialis anterior motoneurones probably representing the 1a IPSP. Excitation, at a latency of 97 ms, may represent spino-bulbo-spinal reflex. None of these effects are due to the excitation of cutaneous afferent nerve fibres.     

Ultrastructure of jaw muscle spindle afferents within the rat trigeminal mesencephalic nucleus

This study examined the ultrastructures of neuronal elements within trigeminal mesencephalic nucleus by labeling masseteric mesencephalic neurons and masseter motoneurons with injection of horseradish peroxidase into masseteric muscle. Of eight horseradish peroxidase-labeled muscle spindle afferents examined, four terminals showed synaptic contact with labeled dendrites of masseteric motoneurons, two with labeled somata, and the remaining two with unlabeled dendrites. A few of the labeled dendrites showed intimate contact with the somata of the trigeminal mesencephalic nucleus neurons. These results provide morphological evidence of synaptic contact of recurring masseteric muscle spindle afferents with the trigeminal mesencephalic nucleus somata and also suggest the presence of electrical synapses between the somata of the trigeminal mesencephalic nucleus neurons and dendrites of jaw-closing motoneurons.     

Interrogating interneurone function using threshold tracking of the H reflex in healthy subjects and patients with motor neurone disease

ObjectiveThe excitability of the lower motoneurone pool is traditionally tested using the H reflex and a constant-stimulus paradigm, which measures changes in the amplitude of the reflex response. This technique has limitations because reflex responses of different size must involve the recruitment or inhibition of different motoneurones. The threshold-tracking technique ensures that the changes in excitability occur for an identical population of motoneurones. We aimed to assess this technique and then apply it in patients with motor neurone disease (MND).MethodsThe threshold-tracking approach was assessed in 17 healthy subjects and 11 patients with MND. The soleus H reflex was conditioned by deep peroneal nerve stimulation producing reciprocal Ia and so-called D1 and D2 inhibitions, which are believed to reflect presynaptic inhibition of soleus Ia afferents.ResultsThreshold tracking was quicker than the constant-stimulus technique and reliable, properties that may be advantageous for clinical studies. D1 inhibition was significantly reduced in patients with MND.ConclusionsThreshold tracking is useful and may be preferable under some conditions for studying the excitability of the motoneurone pool. The decreased D1 inhibition in the patients suggests that presynaptic inhibition may be reduced in MND.SignificanceReduced presynaptic inhibition could be evidence of an interneuronopathy in MND. It is possible that the hyperreflexia is a spinal pre-motoneuronal disorder, and not definitive evidence of corticospinal involvement in MND.     

Synaptic effects from chemically activated fine muscle afferents upon α-motoneurones in decerebrate and spinal cats

In spinal and decerebrate cats fine muscle afferents (group III and IV) were selectively activated by intra-arterial injection of bradykinin and KCl into the gastrocnemius-soleus muscle. By this method the synaptic responses induced in lumbar α-motoneurones by fine muscle afferents could be examinedwithout interference of effect from large afferents. α-Motoneurones receiving EPSPs evoked by electrical stimulation of cutaneous and high threshold muscle afferents (mainly flexor motoneurones) responded to the activation of fine muscle afferents with a depolarization of their membrane and an increase in synaptic noise, while motoneurones in which IPSPs were evoked by electrical stimulation of cutaneous and high threshold muscle afferents (mainly extensor motoneurones), responded with hyperpolarization of their membrane. Cells with mixed excitatory-inhibitory electrically induced response characteristic responded with an increase in synaptic noise without substantial change in the level of their membrane potential to chemical stimulation of fine muscle afferents. The results indicate that one function of group IIIand IV muscle afferents is to participate in the complex reflex control performed by the flexor reflex system.     

Crossed and uncrossed synaptic actions on motoneurones of back muscles in the cat

Intracellular recording from motoneurones of back muscles was used to analyze their synaptic input. The sample included motoneurones located in Th13--L2 spinal segments, identified by their antidromic invasion following stimulation of medial, intermediate and lateral branches of the dorsal rami. The motoneurones were monosynaptically excited from lowest threshold ipsilateral afferents and from ipsilateral descending spinal tracts. Polysynaptic EPSPs and/or IPSPs were evoked in them from higher threshold ipsilateral and contralateral afferents and from descending spinal tracts, and recurrent inhibition was evoked from ipsilateral motor axon collaterals. There was no evidence of crossed disynaptic inhibition from group I afferents, or crossed recurrent inhibition of these neurones. Supplementary records from another group of neurones in Th13--L2 segments, unidentified but likely to innervate other back or abdominal muscles, showed monosynaptic and polysynaptic PSPs of the same origin, and in addition disynaptic IPSPs and disynaptic EPSPs from contralateral ventral roots. The crossed IPSPs had features of the crossed recurrent IPSPs, while the crossed EPSPs appeared to be more likely evoked by some afferents passing via the ventral roots. Generally, the input to the investigated neurones showed greatest similarities to the input to motoneurones of neck muscles and differed from that reported for tail motoneurones.