Experimental jaw-muscle pain does not change heteronymous H-reflexes in the human temporalis muscle

Muscle pain generally has an inhibitory effect on voluntary orofacial motor function. However, it is not known whether muscle pain causes direct or indirect changes in motoneuron excitability. In this study a monopolar needle stimulation technique was used to evoke the direct motor response (M-response) in the left masseter muscle and the heteronymous H-reflex in the left temporalis muscle as an indirect measure of motoneuron excitability. Series of 20 repeated electrical stimuli were delivered at 50% of maximal voluntary contraction (MVC) before, during, and after periods with experimental jaw-muscle pain in 11 healthy subjects. Pain was induced by standardized infusion of hypertonic (5%) saline into the mid-portion of the right masseter muscle. The mean pain intensity rating on a 100-mm visual analog scale was 42±5 mm. The short-latency responses (less than 6 ms) could be evoked in all subjects. Analysis of the latency and amplitude of the temporal H-reflex indicated no significant effect of jaw-muscle pain. The amplitude of the masseteric M-response was significantly smaller in the postpain condition than in the pain conditions (ANOVA, P=0.018), but no differences were found between the prepain and postpain conditions. In nine subjects, poststimulus periods (mean offset latency, 69.6±8.6 ms) with significantly (more than 50%) suppressed EMG activity were detected in the ipsilateral masseter muscle following the M-response (mean offset latency, 5.5±0.2 ms). These reflex responses did not show a systematic change during the pain conditions. In conclusion, acute contralateral jaw-muscle pain does not seem to modulate the motoneuron excitability as measured by the heteronymous H-reflex. Received: 7 November 1997 / Accepted: 16 February 1998     

Conditioning of heteronymous H reflex in human temporalis muscle by stimulation of perioral afferents

A heteronymous H reflex in the temporalis muscle can be elicited by selective stimulation of the masseteric nerve. The present study aimed at defining the optimal amplitude of the H reflex to detect inhibitory changes induced by stimulation of the perioral afferents and at providing new information on the control of masticatory muscles. Sixteen healthy volunteers participated in the experiment. A conditioning stimulus (CS) to the perioral skin was applied at various delays before an ipsilateral selective masseteric nerve stimulation (test stimulus: TS) while the subject was clenching the teeth at 25% of the maximal voluntary contraction. Two intensities of CS and TS were employed, high and low. The peak-to-peak amplitude of the H reflex (TS) and the root-mean-square value of the preceding electromyography were measured and the data analyzed by three-way analysis of variance and Tukey's posthoc tests. For both intensities used the heteronymous H reflex in the temporalis muscle was significantly decreased by prior activation of perioral afferents for delays from 5 to 60 ms. With a delay of 5 and 35 ms the preceding EMG level was not changed, while it was reduced at 20 and 60 ms delay. The intensities used to elicit the heteronymous H reflex of the temporalis muscle were appropriate to detect a reduction in motoneuron excitability. The reduction in the H reflex without a change in the preceding EMG at 5 and 35 ms delays could be due to presynaptic inhibition of the masseteric afferents exerted by the ipsilateral perioral afferents.     

Regional differences in fibre type composition in the human temporalis muscle

Anatomical and electromyographic studies point to regional differences in function in the human temporalis muscle. During chewing and biting the anterior portions of the muscle are in general more intensively activated and they are capable of producing larger forces than the posterior portions. It was hypothetised that this heterogeneity in function is reflected in the fibre type composition of the muscle. The composition and surface area of different fibre types in various anteroposterior portions of the temporalis muscle were investigated in 7 cadavers employing immunohistochemistry with a panel of monoclonal antibodies against different isoforms of myosin heavy chain. Pure slow muscle fibres, type I, differed strongly in number across the muscle. In the most posterior portion of the muscle there were 24% type I fibres, in the intermediate portion 57%, and in the most anterior portion 46%. The mean fibre cross-sectional area (m-fcsa) of type I fibres was 1849 μm², which did not differ significantly across the muscle. The proportion of pure fast muscle fibres, type IIA and IIX, remained more or less constant throughout the muscle at 13% and 11% respectively; their m-fcsa was 1309 μm² and 1206 μm², respectively, which did not differ significantly throughout the muscle. Pure type IIB fibres were not found. The relative proportion of hybrid fibres was 31% and did not differ significantly among the muscle portions. Fibre types I+IIA and cardiac α+I+IIA were the most abundant hybrid fibre types. In addition, 5% of the type I fibres had an additional myosin isoform which has only recently been described by means of electrophoresis and was named Ia. In the present study they were denoted as hybrid type I+Ia muscle fibres. It is concluded that intramuscular differences in type I fibre distribution are in accordance with regional differences in muscle function.     

Tendon entheses of the human masticatory muscles

Tendons attach to the limb skeleton via chondral-apophysary or periosteal-diaphysary entheses. It was the aim of the present study to investigate the tendon entheses of the temporal, the masseter, as well as the medial and lateral pterygoid muscles, considering the biomechanics and the mode of osteogenesis at the attachment sites. The origin and insertion zones of the four masticatory muscles were studied histologically and by polarization light microscopy in six halves of human heads. Contrary to the limb skeleton no causal relationship between the histological structure of the tendon entheses and the osteogenic mode of the bone areas involved was observed in the masticatory muscles that were studied. Based on the histological findings, a purely structural classification of the tendon attachments irrespective of the osteogenesis is therefore proposed that is applicable to the entire skeleton. It is possible to distinguish between tendon entheses inserting into periosteum, into bone or into fibrocartilage. Tendon attachments with periosteal insertion are found at the temporal plane, the retromolar triangle, zygomatic arch, lateral pterygoid plate, in the caudal zone of the pterygoid fovea of the neck of mandible as well as major portions of the ramus and angle of the mandible. The attachment zones in which collagen fibrils of tendons insert into the bone via the periosteum correspond in their structure to plane periosteal-diaphysary insertions into the diaphyses of long bones. Attachment zones to the bone are present at the inferior temporal line, the base of the coronoid process, the caudal surface of the zygomatic arch, the cranial zones of the pterygoid fovea of the neck of the mandible as well as at circumscribed areas of the ramus and angle of the mandible. In these zones the collagen fibers of the tendon insert immediately into the bone without any mediation of other tissues. The entheses resemble those of circumscribed periosteal-diaphysary attachments to long bones. Fibrocartilaginous entheses occur at the coronoid process, the cranialmost portions of the pterygoid fovea of the neck of the mandible as well as in circumscribed areas of the medial and lateral facets of the angle of the mandible. The structures of these attachment sites are comparable to chondral-apophysary tendon attachments. As for masticatory muscles, the described forms of tendon entheses occur at the same time in the majority of the attachment sites. From the structure of the three types of tendon entheses it is possible to conclude that they fulfill a biomechanical function similar to that of the limb skeleton, namely adapting the different elasticity moduli of bone and tendon tissues. From a technical perspective they can be considered to act as an ”angle and stretching brake”. Accepted: 29 March 2000     

Modulation of motor unit discharge rate and H-reflex amplitude during submaximal fatigue of the human soleus muscle

Declining motor unit discharge rates and H-reflex amplitude have been observed in separate experiments during fatiguing submaximal contractions in humans. The purpose of this experiment was to investigate motor unit discharge rate, H-reflex amplitude, and twitch contractile properties concurrently during a fatiguing submaximal isometric contraction of the ankle plantarflexors. Eleven healthy subjects performed fatiguing contractions of low force (25% maximal voluntary contraction (MVC)) or high force (42–66% MVC). Hoffmann (H)-reflexes, muscle compound action potentials (M-waves), twitch contractile properties, and motor unit discharges were recorded from the soleus muscle. In the low-force fatigue task, motor unit firing rate increased gradually over time, whereas the resting H-reflex was significantly depressed at 15% of endurance time and remained quasiconstant for the rest of the task. This suggests that the processes mediating the resting H-reflex depression are relatively independent of those modulating the motor unit firing rate during a low-force fatigue task. In the high-force fatigue task, a decline in the average motor unit discharge rate was accompanied by a decrease in the resting H-reflex amplitude and a prolongation of the twitch half-relaxation time (HRT) at the completion of the fatigue task. Overall, motor unit firing rate was modulated in parallel with changes in the twitch HRT, consistent with the muscle wisdom hypothesis.     

Cyclic modulation of the H-reflex in a wrist flexor during rhythmic flexion-extension movements of the ipsilateral foot

 In 12 subjects, each sitting on an armchair with the right forearm prone, the H-reflex elicited in the resting flexor carpi radialis muscle underwent cyclic excitability changes correlated with rhythmic flexion-extension movements of the ipsilateral foot (frequency of oscillations between 1.5 and 2.5 Hz). During foot plantar flexion, the H-reflex underwent a clear-cut increase, the maximum facilitation falling, in most subjects, within the second half of that phase; then, a gradual reduction in size led the reflex amplitude back to the initial value at the end of foot dorsal extension. If present also when the wrist and the ankle are moved together, this facilitation should favour the in-phase (isodirectional) association between movements and, conversely, hinder the anti-phase coupling. Received: 16 June 1997 / Accepted: 10 July 1997     

The time-course of preparatory spinal and cortico-spinal inhibition: an H-reflex and transcranial magnetic stimulation study in man

 In a previous study where reaction-time methods were combined with transcranial magnetic stimulation (TMS) of the motor cortex, cortico-spinal excitability was shown to reflect time preparation. Provided that subjects can accurately estimate time, the amplitude of motor-evoked potentials (MEPs) diminish progressively during the interval separating the warning signal from the response signal (i.e., the foreperiod). On the other hand, several experiments have demonstrated that the amplitude of the Hoffman (H) reflex elicited in prime movers diminishes during the foreperiod of reaction-time tasks. The aim of the present study was to compare the time course of the respective decrements of H-reflex and MEP amplitude during a constant 500-ms foreperiod. The subjects (n=8) participated in two experimental sessions. In one session, H-reflexes were induced in a tonically activated, responding hand muscle, the flexor pollicis brevis, at different times during the foreperiod of a visual-choice reaction-time task. In the other session, motor potentials were evoked in the same muscle by TMS of the motor cortex delivered in the same behavioral conditions and at the same times as in the first session. The results show that both H-reflexes and MEPs diminish in amplitude during the foreperiod, which replicates and extends previous findings. Interestingly, the time constants of the two decrements differed. There was a facilitatory effect of both electrical and magnetic stimulations on the subject’s performance: reaction time was shorter for the trials during which a stimulation was delivered than for the no-stimulation trials. This facilitation was maximal when the stimulations were delivered simultaneously with the warning signal and vanished progressively with stimulation time. Received: 6 November 1997 / Accepted: 2 June 1998     

Recruitment of extensor-carpi-radialis motor units by transcranial magnetic stimulation and radial-nerve stimulation in human subjects

The responses of 34 extensor-carpi-radialis motor units to graded transcranial magnetic stimulation (TMS) and electrical stimulation of the radial nerve were investigated in six human subjects. Simultaneously with the recording of the single motor-unit discharges, motor-evoked potentials (MEPs) and H-reflexes evoked by the two types of stimulation were recorded by surface electrodes and expressed as a percentage of the maximal motor response (Mmax). Ten motor units were activated in the H-reflex when it was less than 5% of Mmax, but not in the MEP even when it was 15% of Mmax. The opposite was observed for three motor units. Eleven motor units were recruited by both stimuli, but with significantly different recruitment thresholds. Only ten motor units had a threshold similar to TMS and radial nerve stimulation. From these observations, we suggest that caution should be taken when making conclusions regarding motor cortical excitability based on changes in the size of MEPs, even when it is ensured that there are no similar changes in background EMG-activity or H-reflexes. Received: 20 November 1998 / Accepted: 4 June 1999     

Effect of ethanol on H-reflex in unanaesthetized rabbits

The effect of ethanol on H-response was observed in 15 unanaesthetized rabbits and five human volunteers. In 25% of the animals there was complete abolition of H-response, 3–5 minutes after intravenous administration of 1 ml/kg body weight of ethanol—blood alcohol concentration (BAC), 160 mg%—whereas in others there was 76–96% depression. However, this depression was transient and after 20 minutes, normal H-reflex could be elicited even when the BAC was 105 mg%. In human volunteers who consumed 250 ml of rum in 30 minutes there was a demonstrable depression 20–30 minutes after they had started alcohol consumption (BAC 120 mg%). However after 60–90 minutes when there were signs of gross motor incoordination, the H-response was normal (BAC 108 mg%). It is concluded that though ethanol has a depressant action on spinal motoneuron function, this cannot account for the motor incoordination of alcohol intoxication.     

Changes in excitability of the flexor carpi radialis H-reflex following tactile stimulation of the index fingertip

Adequate stimulation of cutaneous afferents from the fingertip evokes a short-latency inhibition followed by a long-lasting excitation in human flexor carpi radialis (FCR) motoneurones. Changes in excitability of flexor motoneurones were investigated in 11 subjects by means of the H-reflex conditioning technique. The index fingertip, immobilised on a flat table, was stimulated by a small probe mounted on an electromagnetic vibrator. Contact time and tactile perception threshold (PT) were monitored throughout the experiment. In all subjects, tactile stimulation of the skin covering the index pulp, with 10 ms long square pulses, at an intensity of 2–2.5 PT, produced an inhibition starting at a conditioning-test interval of 15 ms and lasting about 2 ms. This was followed by a powerful facilitation lasting more than 10 ms. Excitation appeared just at tactile threshold, whereas threshold for inhibition was about 2 PT. Similar effects were observed after mechanical stimulation of the skin covering the dorsal aspect of the index, close to the nail. Local anaesthesia of the finger pulp drastically reduced both the inhibition and the facilitation of FCR H-reflex. By contrast, electrical stimulation of the index digital nerves, by means of ring electrodes, was always ineffective in modifying the excitability of the FCR H-reflex. It is proposed that inhibition and excitation of FCR H-reflex are caused by activation of oligosynaptic pathways fed by cutaneous afferents; however, it cannot be excluded that joint receptors and primary endings of small hand muscles may contribute in part to the late excitation. The pathways described might play an essential role in modulation and control of exploratory movements and object manipulation, actions that need tactile information to regulate muscle force. Received: 30 June 1997 / Accepted: 3 November 1997     

Movements modulate the reflex responses of human flexor pollicis longus to stretch

The reflex responses to brisk, ramp stretch perturbations of the human flexor pollicis longus muscle (FPL) were recorded during isometric and slow concentric or eccentric contractions at similar levels of muscle excitation. The subjects flexed their thumb to push down against a thumb-rest, whose position was controlled by a servo-controlled motor. In different runs, the stretch perturbations were imposed when the thumb-rest was stationary (isometric) or was flexing or extending the interphalangeal joint of the thumb at a constant velocity, i.e. during concentric or eccentric contractions of FPL. The latency of the most prominent component of the electromyographic reflex in the isometrically contracting muscle was about 60 ms, measured from the command signal. The amplitude of this response was sharply reduced during the non-isometric contractions. While not dependent on the direction, this modulation of the reflex response increased with the speed of active movement of the interphalangeal joint (flexion or extension). The response was greatly reduced during concentric or eccentric movements as slow as 1.6 mm·s^–1 (approximately 5°·s^–1 at the joint). When the force rather than the position of the thumb-rest was servo-controlled, the stretch response to perturbation again diminished with speed in a self-paced flexion task, compared with an isometric “hold” condition. Received: 25 April 1996 / Accepted: 2 June 1997     

Dynamic changes in corticospinal excitability during motor imagery

 We investigated temporal changes in the amplitudes of motor-evoked potentials (MEPs) induced by transcranial magnetic stimulation over the left motor cortex during motor imagery. Nine subjects were instructed to imagine repetitive wrist flexion and extension movements at 1 Hz, in which the flexion timing was cued by a tone signal. Electromyographs (EMGs) were recorded from the first dorsal interosseous, flexor carpi radialis and extensor carpi radialis muscles of the right hand, and magnetic stimulation was delivered at 0, 250, 500 and 750 ms after the auditory cue. On average, the evoked EMG responses were larger in the flexor muscle during the phase of imagined flexion than during extension, whilst the opposite was true for the extensor muscle. There were no consistent changes in the amplitudes of MEPs in the intrinsic hand muscle (first dorsal interosseous). The EMG remained relaxed in all muscles and did not show any significant temporal changes during the test. The H-reflex in the flexor muscle was obtained in four subjects. There was no change in its amplitude during motor imagery. These observations lead us to suggest that motor imagery can have dynamic effects on the excitability of motor cortex similar to those seen during actual motor performance. Received: 23 July 1998 / Accepted: 26 October 1998     

Motor coordination in a multi-muscle system as revealed by principal components analysis of electromyographic variation

The variation in electromyographic output of twelve trigeminal muscles of the rabbit was studied to test the hypothesis that they are under the control of a small number of independent neural factors. Jaw muscle electromyograms (EMGs) of eight animals were recorded in 95 chewing sequences, each consisting of 40–75 chewing cycles. The within-sequence correlations of the EMG burst amplitudes (integrated per cycle) and burst onsets were calculated between the muscles. The correlation matrix was subjected to a principal components analysis. This method aims at describing the variation in EMG amplitude and timing by means of the smallest possible set of newly defined variables, or principal components. Of the variation in EMG amplitude values of the twelve muscles, 75–90% could be accounted for by only three principal components. Each principal component was characterized by a group of muscles with high mutual positive correlations; they had zero correlation with other principal components. The first component represents the jaw closers: most of the bilateral masseter and the medial pterygoid muscles. The second represents the openers: the bilateral digastric and lateral pterygoid muscles. This demonstrates the tight control of both the jaw openers and closers, each by a single neural factor; these two factors are independent of one another. They most likely originate from the specific inputs from primary afferents to the opener and closer motoneurons. Unexpectedly, a third independent principal component appeared to control the closing activity of the non-chewing side, posterior deep masseter muscle. It was hypothesized that this muscle acts independently of the other closers to disengage the teeth and resets the jaw for a new chewing cycle. Principal components analysis of variation in timing of EMG onset revealed a grouping of all masticatory muscles in a single cluster, independent of EMG amplitude. This supports the hypothesis that timing and amplitude of masticatory EMG patterns are controlled independently. Received: 16 January 1998 / Accepted: 15 March 1999     

Comparison of the depression of H-reflexes following previous activation in upper and lower limb muscles in human subjects

 When conditioning-testing (C-T) stimuli are applied to Ia afferents to elicit H-reflexes, the test reflex is abolished immediately following the conditioning reflex. As the C-T interval is increased, the test response slowly begins to recover, taking several hundred milliseconds to attain control values. The time course of this recovery is known as the H-reflex recovery curve. H- reflex recovery curves were compared using surface EMG and single motor unit activities in lower limb soleus and upper limb flexor carpi radialis (FCR) muscles in seven healthy human subjects. Under rest conditions, the recovery of H-reflexes and single motor unit activity was slow for soleus; the recovery was not complete even in 1 s. In comparison, the recovery was very fast for FCR motor units, occurring in 200–300 ms. The effects of rate of stimulation (0.1–10.0 imp/s) were also examined on the magnitude of H-reflex responses. The reflex response declined with increasing rate of stimulation, the decline being slightly greater in soleus than in FCR. When these phenomena were examined with voluntary facilitation of the spinal cord, the time of recovery shortened and the effect of stimulus rate also diminished. Changes with background facilitation were greater in FCR than in soleus. The differences between the two muscles are attributed mainly to differences in presynaptic inhibition in the two spinal segments, and/or to the differences in dynamics of the transmitter release in terminals of Ia afferents synapsing with slow soleus motoneurons and those synapsing with the fast FCR motoneurons. Received: 23 April 1998 / Accepted: 6 November 1998     

Effects of changes in hip joint angle on H-reflex excitability in humans

We examined the amplitude modulation of the soleus (Sol) H-reflex during controlled variations of the hip joint angle in 21 healthy adult human subjects. Hip angle variations were imposed separately, or in combination either with stimulation of the plantar skin or with electrical activation of muscle afferents from the medial gastrocnemius (MG) nerve. We found that with subjects in the supine position, flexion of the hip significantly depressed Sol H-reflex excitability, by as much as 50% of control reflex values (Ho) recorded at 10 degrees of hip flexion. Conversely, significant facilitation of the H-reflex was observed when the hip joint was extended (10 degrees), with amplitudes reaching 200+/-15.3% of Ho. Changes in H-reflex amplitude were also observed during electrical stimulation of either the foot sole or the MG nerve, when stimuli were delivered at different hip angles. Foot sole stimulation resulted in facilitation of the H-reflex with the hip extended while depression of the reflex was recorded with the hip flexed. In contrast, MG nerve stimulation at group-I muscle afferent strength resulted in a significant increase in the Sol H-reflex magnitude with the hip flexed, while during hip extension, no significant effects were observed [corrected]. This study provides evidence for the existence of a spinal mechanism, determined principally by the hip joint angle, which promotes switching between inhibitory and facilitatory pathways during hip flexion and extension. The origins of such a spinal mechanism are discussed.     

Innervation of the human lateral pterygoid muscle

The one- or two-headed arrangement of the lateral pterygoid m. (LPM) was analysed by studying the motor nerve distribution within the muscular tissue. In all subjects, the main innervation of the lateral pterygoid m. came from the anterior trunk of the mandibular n. by one to three nerves. These nerves divided into five or six vertical branches which ramified into parallel horizontal tiny fibers. Consequently, the lateral pterygoid m. appeared to be divided into oblique sagittal planes and horizontal layers by the nerve branches, reflecting the multipennate organisation of the muscle. These layers can be selectively recruited during mandibular movements, ensuing a fine medial-lateral control. According to its nerve supply, the LPM has to be considered as a single unit made of independent functional musulo-aponeurotic layers even though its morphologic conformation is in one, two or three heads.     

Facilitation of muscle evoked responses after repetitive cortical stimulation in man

The technique of repetitive transcranial magnetic stimulation (rTMS) allows cortical motor areas to be activated by trains of magnetic stimuli at different frequencies and intensities. In this paper, we studied long-term neurophysiological effects of rTMS delivered to the motor cortex at 5 Hz with an intensity of 120% of motor threshold. Each stimulus of the train produced muscle-evoked potentials (MEPs) in hand and forearm muscles, which gradually increased in size from the first to the last shock. After the end of the train, the response to a single-test stimulus remained enhanced for 600–900 ms. In contrast, the train had no effect on the size of the MEPs evoked by transcranial electrical stimulation, while it suppressed H-reflexes in forearm muscles for 900 ms. We conclude that rTMS of these parameters increases the excitability of the motor cortex and that this effect outlasts the train for almost 1 s. At the spinal level, rTMS may increase presynaptic inhibition of Ia afferent fibers responsible for the H-reflex. Received: 12 November 1997 / Accepted: 23 February 1998     

Effect of prematurity and intrauterine growth restriction on H-reflex recovery cycle in neonates

Objective: The purpose of this work was to assess the effects of prematurity and intrauterine growth restriction on spinal cord synapses using H-reflex. Methods: 33 babies were investigated at birth. 14 were full term appropriate for gestational age (FT AGA), 10 were full term intrauterine growth restricted (FT IUGR) and 9 were preterm appropriate for gestational age (PT AGA). The maximum amplitude of H-reflex (Hmax), H-reflex latency (HRL), H/M ratio, H-reflex conduction velocity (HRCV), and H-reflex response to double stimuli (conditioning and test) for H-reflex recovery cycle (HRRC) were recorded in right lower limb (soleus muscle) in all the three groups. Results: Percentage recovery values of H-reflex were significantly higher in FT AGA and FT IUGR babies compared to PT AGA neonates for most of inter-stimulus intervals. No significant differences were observed in H-reflex parameters between FT AGA and FT IUGR groups, but HRL and HRCV were significantly affected in PT AGA group. Conclusions: Delayed H-reflex recovery in preterms may be due to a prolonged state of neurotransmitter delay in Ia terminals following initial activation by the conditioning stimuli. The cause of such prolonged depletion of neurotransmitters could be attributed to a poor neurotransmitter store in synaptic vesicles of spinal cord in preterm neonates.