Asymmetric activation of motor cortex controlling human anterior digastric muscles during speech and target-directed jaw movements.

Like most of the cranial muscles involved in speech, the trigeminally innervated anterior digastric muscles are controlled by descending corticobulbar projections from the primary motor cortex (M1) of each hemisphere. We hypothesized that changes in corticobulbar M1 excitability during speech production would show a hemispheric asymmetry favoring the left side, which is the dominant hemisphere for language processing in most strongly right handed subjects. Fifteen volunteers aged 24.5+/-5.3 (SD) yr participated. All subjects were strongly right handed as reported by questionnaire. A surface electromyograph (EMG) was recorded bilaterally from digastrics and jaw movement detected by an accelerometer attached to a lower incisor. Focal transcranial magnetic stimulation (TMS) was used to assess corticomotor excitability of the digastric representation in M1 of both hemispheres during four tasks: 1) static isometric contraction of digastrics; 2) speaking a single word; 3) visually guided, nonspeech jaw movement that matched the jaw kinematics recorded during task 2; and 4) reciting a sentence. Background EMG was well matched in all tasks and jaw kinematics were similar around the time of the TMS pulse for tasks 2-4. TMS resting thresholds and digastric muscle-evoked potential (MEP) size during isometric contraction did not differ for TMS over left versus right M1. MEPs elicited by TMS over left, but not right M1 increased in size during speech and nonspeech jaw movement compared with isometric contraction. We conclude that left corticobulbar M1 is preferentially engaged for descending control of digastric muscles during speech and the performance of a rapid jaw movement to match a target kinematic profile.

Motor training decreases finger tremor and movement response time in a visuomotor tracking task.

The authors sought to determine whether repeated practice of a skilled motor task reduced the tremor arising from pulsatile control that occurs during and after training. Participants flexed and extended their index finger at the metacarpophalangeal joint to track a screen cursor during skill training, in 6 training runs, each of 3-min duration. Nonskill training comprised voluntary flexion and extension movements. The authors measured performance by the average tracking error in a standard 10-s target pattern embedded in the training runs. Cross-correlation of the motor performance and the target pattern revealed that the improved ability to match the shape of the target pattern accounted for 63% of the improved motor performance and that the decreased time to respond to changes in the target line accounted for 10% of the improvement. Skill, but not nonskill training, reduced tremor after 3 min of training during the training movements and during movements 10 and 25 min afterwards. The authors observed no changes in resting tremor after either training protocol. Although training reduced the tremor, this reduction in itself did not significantly improve tracking performance. The authors conclude that visuomotor skill training produces a general reduction in finger tremor (pulsatile control) during voluntary movements that extends beyond the period of training.

Transcranial magnetic stimulation reduces masseter motoneuron pool excitability throughout the cortical silent period.

OBJECTIVE: To evaluate the time-course of changes in masseter motoneuron pool excitability following transcranial magnetic stimulation of motor cortex, and relate this to the duration of the masseter cortical silent period (CSP). METHODS: Surface EMG was recorded bilaterally from masseter and digastric muscles in 13 subjects. Focal TMS was applied at 1.3x active motor threshold (AMT) to motor cortex of one hemisphere to elicit a muscle evoked potential (MEP) and silent period bilaterally in masseter as subjects maintained an isometric bite at approximately 10% maximum. With jaw muscles relaxed, a servo-controlled stretcher evoked a stretch reflex in masseter which was conditioned by TMS (1.3x AMT) at 14 different conditioning-testing intervals. There were 20 trials at each interval, in random order. TMS evoked no MEP in resting masseter, but often produced a small MEP in digastric. RESULTS: Mean (+/-SE) masseter CSP was 67+/-3ms. The masseter stretch reflex was facilitated when stretch preceded TMS by 8 and 10ms, which we attribute to spatial summation of corticobulbar and Ia-afferent excitatory inputs to masseter. Masseter stretch reflex amplitude was reduced when TMS was given up to 75ms before stretch, and for up to 2ms afterwards. CONCLUSIONS: We conclude that descending corticobulbar activity evoked by TMS acts bilaterally on brainstem interneurons that either inhibit masseter motoneurons or increase pre-synaptic inhibition of Ia-afferent terminals for up to 75ms after TMS. The reduction of masseter motoneuron pool excitability following TMS has a similar time-course to the CSP. SIGNIFICANCE: In contrast to the situation for spinal and facial (CN VII) muscles, the masseter CSP appears to have no component that can be attributed exclusively to cortical mechanisms. Abnormalities in the masseter cortical silent period observed in neurological conditions may be due to pathophysiological changes at cortical and/or sub-cortical levels.

Focal transcranial magnetic stimulation of motor cortex evokes bilateral and symmetrical silent periods in human masseter muscles.

OBJECTIVE: To determine whether a single hemisphere exerts distinct inhibitory influences over masseter muscles on each side, and to compare features of the masseter cortical silent period (CSP) evoked by transcranial magnetic stimulation (TMS) with previous reports from limb and other cranial muscles. METHODS: Focal TMS was applied over the motor cortex jaw area in 14 normal subjects. In one experiment, TMS intensity was constant (1.1 or 1.3x active motor threshold, T) and masseter muscle activation varied from 10% to 100% of maximal. In another experiment, muscle activation was constant (20% maximal) and TMS intensity varied from 0.7 to 1.3T. RESULTS: In all subjects, TMS evoked a silent period of similar duration in masseter muscles on both sides. Masseter CSP duration increased at higher TMS intensities, but was not affected by muscle activation level or the size of the excitatory response evoked by TMS. Weak TMS produced a bilateral CSP without short-latency excitation. The masseter CSP was short ( approximately 100ms at 1.3T), yet this was not due to maintenance of excitatory drive from the unstimulated hemisphere, as the masseter CSP was not prolonged with dual-hemisphere TMS. CONCLUSIONS: Intracortical inhibitory circuits activated by TMS have a relatively weak effect on corticotrigeminal neurons supplying masseter, and effects are equivalent for corticobulbar efferents directed to contralateral and ipsilateral masseter motoneuron pools. SIGNIFICANCE: Trigeminally innervated masseter muscles exhibit weak, bilaterally symmetric inhibition following focal TMS. This method can be used to investigate abnormalities of intracortical inhibition in movement disorders or focal lesions affecting the masticatory muscles in humans.

Investigation of an unusual, high-frequency jaw tremor with coherence analysis.

Normal physiological tremor of the jaw has a frequency of 6 to 8 Hz. A patient is described with jaw tremor at frequencies of 12 Hz during jaw movement and 15 Hz when the jaw was relaxed. The 15 Hz tremor was driven by synchronous, bilateral bursts of activity in the temporalis and masseter muscles, which alternated with digastric bursts. Coherence analysis indicated the tremor was highly correlated with both opening and closing muscle activity, and that the opening and closing muscles were about 180 degrees out of phase. The existence of two tremors with different, nonphysiological peak frequencies and the influence of attention, relaxation, and movement in switching from one tremor frequency to the other, suggest that more than one generator may be operating.

Intracortical inhibition in the human trigeminal motor system.

OBJECTIVE: To investigate the presence and features of short-interval intracortical inhibition (SICI) in the human trigeminal motor system. METHODS: Surface electromyogram (EMG) was recorded from left and right digastric muscles in 7 subjects, along with additional experiments with intramuscular EMG in 2 subjects. Focal transcranial magnetic stimulation (TMS) was used to activate the motor cortex of one hemisphere and elicit motor evoked potentials (MEPs) in digastric muscles on each side, at rest and while subjects activated the muscles at 10% maximal EMG. Paired or single TMS pulses were delivered in blocks of trials, while conditioning TMS intensity and interstimulus interval (ISI) were varied. RESULTS: At rest, paired TMS (3-ms ISI) with conditioning intensities 0.8-0.9x active motor threshold (TA) reduced the digastric MEP amplitude to a similar extent bilaterally. Conditioning at 0.5-0.7TA did not significantly reduce the MEP. MEP amplitude was reduced to a similar extent in both digastric muscles by ISIs between 1 and 4 ms (0.8TA). Voluntary bilateral activation of digastric muscles reduced the effectiveness of conditioning TMS compared to the resting state, with no differences between sides. The similarity of the responses in both digastric muscles was not due to EMG cross-talk (estimated to be approximately 10% in surface records and approximately 2% in intramuscular records), as the intramuscular records showed the same pattern as the surface records. CONCLUSIONS: The effects of paired-pulse TMS on digastric are similar to those reported for contralateral hand muscles, and are consistent with activation of SICI circuits in M1 by conditioning TMS. Our evidence further suggests that the corticomotor representations of left and right digastric muscles in M1 of a single hemisphere receive analogous inhibitory modulation from SICI circuits. SIGNIFICANCE: SICI has been demonstrated in the face area of motor cortex controlling the trigeminal motor system in normal subjects. This method can be used to investigate abnormalities of SICI in movement disorders affecting the masticatory muscles in humans.

Influence of combined afferent stimulation and task-specific training following stroke: a pilot randomized controlled trial.

BACKGROUND: Reorganization of the human motor cortex can be induced by specific patterns of peripheral afferent stimulation. The potential for afferent stimulation to facilitate the functional recovery associated with conventional rehabilitative techniques has not previously been investigated. OBJECTIVE: The authors sought to determine whether combining appropriate afferent stimulation with task-specific training resulted in greater improvements than training alone in patients with impaired upper limb function in the subacute phase following stroke. METHOD: Twenty patients with hemiparesis due to stroke were allocated randomly to either a stimulation or control group. All received 9 sessions of task-specific physiotherapy training over 3 weeks. Prior to each training session, associative electrical stimulation of the motor point of 2 hand muscles was given in the stimulation group, whereas the control group received sham stimulation. Changes in dexterity were assessed using a grip-lift task, and standard measures of upper-limb function were made before and following the intervention. Corticospinal excitability was examined using transcranial magnetic stimulation. RESULTS: Both groups showed comparable improvements in functional measures of upper-limb function. Of the 20 patients, only 14 could perform the grip-lift task, which is an objective measure of dexterity. Patients in the stimulation group exhibited significantly greater improvements in this task than the control group. There was no significant change in corticospinal excitability in either group. CONCLUSION: This pilot study provides preliminary data suggesting that targeted afferent stimulation may facilitate the response to conventional rehabilitation in patients with hemiparesis due to stroke, but these results need to be confirmed in a larger scale study.

Postural control of the human mandible.

This article reviews recent experimental evidence explaining the mechanisms that support the mandible in its rest or postural position when the head is stationary and during locomotion. At rest, and during slow jaw movements, there is alternating activation of the jaw-opening and jaw-closing muscles which arises from a central pattern generator. However, this cannot account for the rest position of the mandible even when the head is stationary. Jaw movements and masticatory muscle activity were measured in subjects who stood, walked and ran on a treadmill. Even during walking, there are no bursts of masseter EMG time-locked to heel-landing. However, when subjects ran, the downward movement of the mandible in each step evokes a burst of EMG in the masseters. This is a stretch reflex in the jaw-closing muscles, which acts to limit the downward movement of the mandible relative to the maxilla during locomotion, and to restore the mandibular position towards its rest position. Thus, when the head is stationary, the low-level activity in the jaw-opening and jaw-closing muscles does not contribute to the rest position. Instead, the mandible is supported by passive viscoelastic forces in perioral soft tissues which limit vertical jaw movements even when the head moves gently up and down during walking. When the head moves more vigorously up and down, stretch reflexes in the jaw-closing muscles limit the movement of the mandible. That is, both passive forces and active reflex responses maintain jaw posture within narrow limits during brisk head movements.

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.

Impairments in precision grip correlate with functional measures in adult hemiplegia.

OBJECTIVE: Analysis of a precision grip-lift task provides measures to assess functional disability of the hand, but the correlation between these measures and accepted tests of motor function in stroke patients has not been established. METHODS: Seventeen subacute stroke patients were studied to compare parameters of a precision grip-lift task between the affected and unaffected side, and to correlate them with function. Functional impairment was assessed with the Action Research Arm Test and the Fugl-Meyer assessment, as well as grip strength and maximal finger-tapping speed. The grip force (GF) and load force (LF) were recorded as patients lifted a custom-built manipulandum. All measures were recorded on two separate occasions, at least 1 week apart. RESULTS: There was good reproducibility between testing sessions for the grip-lift and functional measures. The affected hand gripped the manipulandum for longer prior to lift-off than the unaffected hand, and the normal close temporal coupling between the rate of change of GF and LF during the lift was disrupted. These two measures correlated more highly with the ARAT than the FMA and, when combined with measures of grip strength and tapping speed, explained 71% of the variance of the ARAT. CONCLUSIONS: The grip-lift task is a sensitive measure of impaired dexterity following stroke and provides measures which correlate well with a commonly applied functional assessment scale. SIGNIFICANCE: This task may be used clinically to detect changes in the hemiplegic upper limb during rehabilitation and recovery.

Experimental muscle pain does not affect fine motor control of the human hand.

Conditions known to cause hand pain, such as arthritis, are often accompanied by impaired dexterity. The aim of this study was to determine whether this association is coincident, or whether pain affects dexterity directly. In the first part of the study, several tests of dexterity based on pegboard skills were compared with a precision-grip-lift task: the correlations between the results of any of these tests were not significant at the 0.01 level. Nineteen subjects were then tested with a modified Purdue pegboard test and the precision grip-lift task, both without pain and during pain induced by injection of 5% hypertonic saline into the first dorsal interosseous muscle of the non-dominant hand. There was no significant difference in the performance of either task when the muscle was painful, indicating that acute experimental muscle pain does not affect dexterity.

Reorganization of the human motor cortex by sensory signals: a selective review.

1. The normal human motor cortex can be made to reorganize by repeated stimulation of proprioceptive inputs, with or without concurrent stimulation of the motor cortex by transcranial magnetic nerve stimulation. Appropriate stimulation induces a focal increase in the excitability of corticospinal projections to specific muscles and, possibly, an increase in the area of the cortex projecting to those muscles. 2. We have shown that repeated stimulation on several successive days causes this 'plastic' reorganization to persist for at least several days. We have also used this approach to determine whether increases in the excitability of the motor cortex can be induced in stroke patients (in whom cortical excitability is usually depressed) and whether this is accompanied by functional changes. 3. The results of these studies were mixed but, in patients in whom plastic changes were induced, there were improvements and sometimes marked improvements in both motor function and some electrophysiological parameters. The reasons for the inconsistent results are not clear, but do not appear to relate to the site, size or nature of the lesion.

Effect of human grip strategy on force control in precision tasks.

Alternate grip strategies are often used for object manipulation in individuals with sensorimotor deficits. To determine the effect of grip type on force control, ten healthy adult subjects were asked to grip and lift a small manipulandum using a traditional precision grip (lateral pinch), a pinch grip with the fingers oriented downwards (downward pinch) and a "key grip" between the thumb and the side of the index finger. The sequence of grip type and hand used was varied randomly after every ten lifts. Each of the three grips resulted in different levels of force, with the key grip strategy resulting in the greatest grip force and the downward pinch grip using the least amount of grip force to lift the device. Cross-correlation analysis revealed that the ability to scale accurately the rate of grip force and load force changes was lowest in the downward pinch grip. This was also associated with a more variable time-shift between the two forces, indicating that the precise anticipatory control when lifting an object is diminished in this grip strategy. There was a difference between hands across all grips, with the left non-dominant hand using greater grip force during the lift but not the hold phase. Further, in contrast with the right hand, the left hand did not reduce grip force during the lift or the hold phase over the ten lifts, suggesting that the non-dominant hand did not quickly learn to optimise grip force. These findings suggest that the alternate grip strategies used by patients with limited fine motor control, such as following stroke, may partly explain the disruption of force control during object manipulation.

Do alternate methods of analysing motor evoked potentials give comparable results?

This study assessed the reliability of alternate methods of analysis of motor evoked potentials (MEPs) elicited by transcranial magnetic stimulation (TMS). We recorded two sets of MEPs (Time 1 and Time 2) at the optimal scalp sites for both the right first dorsal interosseous (FDI) and flexor carpi ulnaris (FCU) at two different stimulation intensities in 10 healthy subjects. MEP magnitude was determined in each of the following three ways: the mean peak-to-peak amplitude and area of the 20 individual responses; the amplitude and area of the ensemble averaged waveform; and the amplitude and area of the maximal response. There was no significant difference in amplitude or area for either muscle using any of the three methods between Time 1 and 2. However, the ensemble average (area and amplitude) was significantly smaller that the mean MEP, and the maximal MEP amplitude was significantly larger. Intraclass correlation analysis demonstrated that reliability of MEP measures over time was poor regardless of method. Reliability was similar between methods for FDI, but FCU had lower reliability values for the mean and ensemble average methods than the maximal method.

Control of human mandibular posture during locomotion.

Mandibular movements and masseter muscle activity were measured in humans during hopping, walking and running to determine whether reflexes contribute to the maintenance of jaw position during locomotion. In initial experiments, subjects hopped so that they landed either on their toes or on their heel. Landing on the toes provoked only small mandibular movements and no reflex responses in the masseter electromyogram (EMG). Landing on the heels with the jaw muscles relaxed caused the mandible to move vertically downwards relative to the maxilla, and evoked a brisk reflex response in the masseter at monosynaptic latency. Neither this relative movement of the mandible nor the reflex was seen when the teeth were clenched: hence the reflex is not the result of vestibular activation during head movement. The same variables were measured in a second series of experiments while subjects stood, walked and ran at various speeds and at various inclinations on a treadmill. During walking, the vertical movements of the head and therefore the mandible were slow and small, and there was no tonic masseter EMG or gait-related activity in the jaw-closing muscles. When subjects ran, the vertical head and jaw movement depended on the running speed and the inclination of the treadmill. Landing on the heels induced larger movements than landing on the toes. About 10 ms after each foot-strike, the mandible moved downwards relative to the maxilla, thereby stretching the jaw-closing muscles and activating them at segmental reflex latency. This caused the mandible to move back upwards. The strength of the reflex response was related to the speed and amplitude of the vertical jaw movement following landing. It is concluded that, during walking, the small, slow movements of the mandible relative to the maxilla are subthreshold for stretch reflexes in the jaw muscles: i.e. the mandible is supported by visco-elasticity of the soft tissues in the masticatory system. However, the brisker downward movements of the mandible after heel-landing during hopping and running evoke segmental reflex responses which contribute to the active maintenance of the posture of the mandible. This is a unique demonstration of how a stretch reflex operates to maintain posture under entirely natural conditions.

Frequency-dependent, bi-directional plasticity in motor cortex of human adults.

OBJECTIVE: To determine whether the plastic changes induced in human motor cortex by afferent stimulation depend on stimulus frequency. METHODS: Transcranial magnetic stimulation was used to examine changes in corticospinal excitability in 20 subjects before and after combined peripheral (motor point) and central stimulation. Peripheral stimuli were given as either low frequency (3 Hz) or high frequency (30 Hz) trains. RESULTS: Low frequency stimulation induced prolonged depression of corticospinal excitability, while high frequency stimulation induced prolonged facilitation. These effects persisted for approximately 40-50 min after stimulation ceased. CONCLUSIONS: Corticospinal plasticity induced by dual peripheral and central stimulation is bi-directionally-modifiable in the adult human, with the direction of change being frequency-dependent. SIGNIFICANCE: Therapies using peripheral stimulation to alter human motor cortex excitability could be tailored to exploit the differential effects of stimulus frequency on the direction of the excitability change.

Postural stability of the human mandible during locomotion.

Movements of the head and of the mandible relative to the head were measured in human subjects walking and running on a treadmill at various speeds and inclinations. A miniature magnet and piezo-electric accelerometer assembly was mounted on the mandibular incisors, and a Hall-effect sensor along with a second accelerometer mounted on a maxillary incisor along a common vertical axis. Signals from these sensors provided continuous records of vertical head and mandible acceleration, and relative jaw position. Landing on the heel or on the toe in different forms of locomotion was followed by rapid deceleration of the downward movement of the head and slightly less rapid deceleration of the downward movement of the mandible, i.e., the mandible moved downwards relative to the maxilla, then upwards again to near its normal posture within 200 ms. No tooth contact occurred in any forms of gait at any inclination. The movement of the mandible relative to the maxilla depended on the nature and velocity of the locomotion and their effects on head deceleration. The least deceleration and hence mandibular displacement occurred during toe-landing, for example, during "uphill" running. The maximum displacement of the mandible relative to the head was less than 1mm, even at the fastest running speed. The mechanisms that limit the vertical movements of the jaw within such a narrow range are not known, but are likely to include passive soft-tissue visco-elasticity and stretch reflexes in the jaw-closing muscles.

Differential modulation of tremor and pulsatile control of human jaw and finger by experimental muscle pain.

Resting tremor is seen in both the limbs and in the trigeminal motor system. These rhythmical perturbations are the result of alternating activation of antagonistic muscles, and these increase in amplitude during slow, voluntary movements. In the present study, we examined the effect of experimental muscle pain on finger and jaw tremor. The tremor in the mandible and in the middle finger was measured on separate occasions, at rest and during two constant-velocity movements. Pain was then induced by the infusion of hypertonic saline into a jaw-closing muscle (masseter) or into a finger extensor muscle (extensor digitorum longus, EDL). During masseter pain, the power at the peak tremor frequency of the mandible decreased significantly both when the jaw was at rest and during voluntary jaw movements at two velocities. In contrast, pain in EDL resulted in a significant increase in the power of finger tremor only during the two speeds of voluntary movement. No change in the peak tremor frequency was seen in either the finger or the jaw during pain. The most likely explanation for these data is that muscle pain tonically modulates the amplitude of the outputs from the central "pulsatile control" generators that drive the alternating activation of antagonistic muscles which produce tremor at rest and during movements. This modulation is in the opposite direction for systems controlling jaw and hand, suggesting a specific interaction of the nociceptive afferents with separate central oscillators.