Periodontal mechanoreceptor input reduces synchronous discharge of voluntarily activated masseter motor units in man

The control exerted by inputs from periodontal mechanoreceptors (PMRs) on the tonic activity of 35 pairs of single motor units in the left masseter muscle was investigated with and without the presence of continuous pressure on the upper left central incisor tooth. Cross-correlograms were computed to assess the temporal coupling between the discharges of the motor unit pairs. In the absence of continuous pressure, central peaks in the cross-correlograms revealed the presence of significant synchronous discharge in 16 out of the 35 pairs tested. In contrast, during PMR stimulation only nine pairs were found to discharge with a significant amount of synchronization. It is concluded that short-term synchronization due to common, partially common and synchronized inputs shared by the motoneurons was reduced whenever extraneous periodontal inputs were superimposed on the voluntary command. This indicates that the interneurons which mediate the periodontal inputs arising from one single tooth are not distributed widely throughout the masseter motoneuron pool. In contrast, it appears that periodontal inputs are liable to reduce the efficiency of common inputs distributed to the masseter motoneurons during voluntary contraction ("desynchronization").     

Masseter EMG activity during sleep and sleep bruxism

The masseter muscle is involved in the complex and coordinated oromotor behaviors such as mastication during wakefulness. The masseter electromyographic (EMG) activity decreases but does not disappear completely during sleep: the EMG activity is generally of low level and inhomogeneous for the duration, amplitude and intervals. The decreased excitability of the masseter motoneurons can be determined by neural substrates for NREM and REM sleep. The masseter EMG activity is increased in association with the level of arousal fluctuations within either sleep state. In addition, there are some motor events such as REM twitches, swallowing and rhythmic masticatory muscle activity (RMMA), whose generation might involve the additional activation of specific neural circuits. Sleep bruxism (SB) is characterized by exaggerated occurrence of RMMA. In SB, the rhythmic activation of the masseter muscle can reflect the rhythmic motor inputs to motoneurons through, at least in part, common neural circuits for generating masticatory rhythm under the facilitatory influences of transient arousals. However, it remains elusive as to which neural circuits determine the genesis of sleep bruxism. Based on the available knowledge on the masseter EMG activity during sleep, this review presents that the variety of the masseter EMG phenotypes during sleep can result from the combinations of the quantitative, spatial and temporal neural factors eventually sending net facilitatory inputs to trigeminal motoneurons under sleep regulatory systems.     

A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions.

Magnetic and electrical stimulation at different levels of the neuraxis show that supraspinal and spinal factors limit force production in maximal isometric efforts ("central fatigue"). In sustained maximal contractions, motoneurons become less responsive to synaptic input and descending drive becomes suboptimal. Exercise-induced activity in group III and IV muscle afferents acts supraspinally to limit motor cortical output but does not alter motor cortical responses to transcranial magnetic stimulation. "Central" and "peripheral" fatigue develop more slowly during submaximal exercise. In sustained submaximal contractions, central fatigue occurs in brief maximal efforts even with a weak ongoing contraction (<15% maximum). The presence of central fatigue when much of the available motor pathway is not engaged suggests that afferent inputs contribute to reduce voluntary activation. Small-diameter muscle afferents are likely to be activated by local activity even in sustained weak contractions. During such contractions, it is difficult to measure central fatigue, which is best demonstrated in maximal efforts. To show central fatigue in submaximal contractions, changes in motor unit firing and force output need to be characterized simultaneously. Increasing central drive recruits new motor units, but the way this occurs is likely to depend on properties of the motoneurons and the inputs they receive in the task. It is unclear whether such factors impair force production for a set level of descending drive and thus represent central fatigue. The best indication that central fatigue is important during submaximal tasks is the disproportionate increase in subjects' perceived effort when maintaining a low target force.     

Synchronization of human motor unit firing during voluntary contraction of muscle and the tonic vibration reflex

We constructed cross-correlograms (CCGs) of action potentials of pairs of motor units (MUs) of human soleus, triceps brachii, and the first and second dorsal interosseous muscles. During voluntary muscle contraction, a pronounced peak in the zero bin was found in 21 out of 126 pairs investigated with the aid of the CCG; this indicates that the number of coincidental firings exceeded chance. The width of the peak did not exceed 5 msec (synchronization for a brief interval, i.e., short-term synchronization). When motoneurons of the soleus muscle were activated by vibration, correlations were found in 12 out 89 pairs of MUs investigated. On the CCGs of action potentials of MU pairs in two muscles (the first and second dorsal interosseous muscles), such correlations were found in four out of 10 pairs investigated. In all of these cases, the ratio of above-change coincidences relative to the total number of MU discharges was small, from 3.0 to 6.1%. Synchronization within a brief time interval can be considered a result of simultaneous creation of EPSPs in motoneourons reached by endings of a single pre-motor nerve fiber. In some pairs of MUs, long term synchronization (clustering) occurred, ie., synchronization lasting several tens of milliseconds. The long-term synchronization can be considered a manifestation of fatigue accompanying tremor.Institute for Problems of Information Transmission, Russian Academy of Sciences, Moscow. Translated from Neirofiziologiya, Vol. 23, No. 6, pp. 691–698, November–December, 1991.     

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

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

用相关分析法研究家兔两类膈神经单位电活动差异的起源

家兔25只,乌拉坦静脉麻醉(1g/kg),三碘季铵酚制动,人工通气,切断双侧颈迷走神经干。分离双侧膈神经,右侧记录神经干放电;左侧分离细束,同时记录一对单位的放电。共记录到36对单位。神经电活动经放大后输入磁带记录仪,备作脱机处理;或将信号放大、限幅后输入计算机,作连机处理。单纤维根据其放电时程同神经干放电的关系分为时相性单位(PU)和紧张性单位(TU)。分别在TU同TU之间、PU同PU之间、PU同TU之间作相关分析。 在总共36对膈运动神经单位对中,有21对的互相关直方图上出现有显著意义的中心峰,表明它们之间存在着同步化活动,是接受共同的中枢传入所致。其中8对为2PU,,11对为2TU,2对为1PU和1TU。同步化活动的类型有短时程同步化、宽峰同步化和高频振荡同步化三种。在同类单位对(2PU或2TU)与不同类单位对(1PU和1TU)出现同步化的频数之间作x~2检验,结果表明同类单位对中出现同步化的比例显著高于不同类的单位对。 据此,我们认为膈运动神经元紧张性单位和时相性单位放电特性的不同可能是由于它们接受不同的中枢支配所致。     

与咬肌运动神经元直接联系的运动前神经元在脑干的分布

目的为了定位向咬肌运动神经元投射的最后一级运动前神经元在脑干内的分布。方法注射麦芽凝集素结合的辣根过氧化物酶(WGA-HRP)至咬肌神经逆行跨突触追踪,然后通过免疫组织化学方法显示了该类神经元。结果这类神经元分布在双侧三叉上核(Vsup)、三叉神经感觉主核背侧部(Vpdm)、小细胞网状结构(PCR)和三叉神经脊束核吻侧亚核背侧部(Vodm),以及对侧三叉神经运动核(Vmo)。数量上,Vsup,特别是注射侧Vsup中,标记的神经元数量最多;其他核团内,双侧标记的神经元的数量无明显差别。结论一侧咬肌运动神经元直接接受脑干双侧多个区域调控。     

Effect of the tendon reflex on motoneurons of the antagonist muscle in man

The knee jerk was elicited during regular firing of relatively low-threshold motor units of the biceps femoris muscle (during weak voluntary contraction). Besides the reflex response of the rectus femoris muscle, synchronous discharges of motor units of the biceps femoris muscle and activation of new motor units also were observed. Poststimulus histograms and statistical analysis of interspike intervals of motor units of the biceps femoris muscle revealed well-marked excitatory influences synchronous with the reflex response of the rectus femoris. This result can be explained by the presence of excitatory inputs of Ia afferents on motoneurons of the antagonist muscle. In the knee jerk, excitation of motoneurons of the antagonist was followed by later inhibitory influences which evidently correspond to the "silent period" of motoneurons of the agonist muscle during the elicitation of its tendon reflex.Institute for Problems of Information Transmission, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 8, No. 6, pp. 624–632, November–December, 1976.     

Synaptic potentials of motoneurons of the masseter muscle

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

The investigation of control mechanisms of stepping rhythm in human in the air-stepping conditions during passive and voluntary leg movements

In unloading condition the degree of activation of the central stepping program was investigated during passive leg movements in healthy subjects, as well as the excitability of spinal motoneurons during passive and voluntary stepping movement. Passive stepping movements with characteristics maximally approximated to those during voluntary stepping were accomplished by experimenter. The comparison of the muscle activity bursts during voluntary and imposed movements was made. In addition to that the influence of artificially created loading onto the foot to the leg movement characteristics was analyzed. Spinal motoneuron excitability was estimated by means of evaluation of amplitude modulation of the soleus H-reflex. The changes of H-reflexes under the fixation of knee or hip joints were also studied. In majority of subjects the passive movements were accompanied by bursts of EMG activity of hip muscles (and sometimes of knee muscles), which timing during step cycle was coincided with burst timing of voluntary step cycle. In many cases the bursts of EMG activity during passive movements exceeded activity in homonymous muscles during voluntary stepping. The foot loading imitation exerted essential influence on distal parts of moving extremity during voluntary as well passive movements, that was expressed in the appearance of movements in the ankle joint and accompanied by emergence and increasing of phasic EMG activity of shank muscles. The excitability of motoneurons during passive movements was greater then during voluntary ones. The changes and modulation of H-reflex throughout the step cycle without restriction of joint mobility and during exclusion of hip joint mobility were similar. The knee joint fixation exerted the greater influence. It is supposed that imposed movements activate the same mechanisms of rhythm generation as a supraspinal commands during voluntary movements. In the conditions of passive movements the presynaptic inhibition depend on afferent influences from moving leg in the most degree then on central commands. It seems that afferent inputs from pressure receptors of foot in the condition of "air-stepping" actively interact with central program of stepping and, irrespective of type of the performing movements (voluntary or passive), form the final pattern activity.     

A Simulation Study to Examine the Effect of Common Motoneuron Inputs on Correlated Patterns of Motor Unit Discharge

The influence of common oscillatory inputs to the motoneuron pool on correlated patterns of motor unit discharge was examined using model simulations. Motor unit synchronization, in-phase fluctuations in mean firing rates known as ‘common drive’, and the coefficient of variation of the muscle force were examined as the frequency and amplitude of common oscillatory inputs to the motoneuron pool were varied. The amount of synchronization, the peak correlation between mean firing rates and the coefficient of variation of the force varied with both the frequency and amplitude of the common input signal. Values for ‘common drive’ and the force coefficient of variation were highest for oscillatory inputs at frequencies less than 5 Hz, while synchronization reached a maximum when the frequency of the common input was close to the average motor unit firing rate. The frequency of the common input signal for which the highest levels of synchronization were observed increased as motoneuron firing rates increased in response to higher target force levels. The simulation results suggest that common low-frequency oscillations in motor unit firing rates and short-term synchronization result from oscillatory activity in different bands of the frequency spectrum of shared motoneuron inputs. The results also indicate that the amount of synchronization between motor unit discharges depends not only on the amplitude of the shared input signal, but also on its frequency in relation to the present firing rates of the individual motor units.     

Influence of nerve supply on hand electromyography coherence during a three-digit task

Intermuscular coupling has been investigated to understand neural inputs to coordinate muscles in a motor performance. However, little is known on the role of nerve innervation on intermuscular coupling. The purpose of this study was to investigate how the anatomy of nerve distribution affected intermuscular coupling in the hand during static grip. Electromyographic (EMG) signals were recorded from intrinsic and extrinsic muscles while subjects performed a static grip. Coherence was computed for muscle pairs innervated by either the same or different nerves. The results did not support the hypothesis that muscles sharing the same nerve exhibit greater coupling than muscles innervated by different nerves. In general, extrinsic muscle pairs displayed higher coherence than intrinsic pairs. The results suggest that intermuscular coupling in a voluntary motor task is likely modulated in a functional manner and that different nerves might transport common neural inputs to functionally coupled muscles.     

Possible mechanisms of muscle cramp from temporal and spatial surface EMG characteristics.

In this study, the initiation and development of muscle cramp are investigated. For this, we used a 64-channel surface electromyogram (EMG) to study the triceps surae muscle during both cramp and maximal voluntary contraction (MVC) in four cramp-prone subjects and during cramp only in another four cramp-prone subjects. The results show that cramp presents itself as a contraction of a slowly moving fraction of muscle fibers, indicating that either the spatial arrangement of the motoneurons and muscle fibers is highly related or that cramp spreads at a level close to the muscle. Spectral analyses of the EMG and peak-triggered average potentials show the presence of extremely short potentials during cramp compared with during MVC. These results can also be interpreted in two ways. Either the motoneurons fire with enlarged synchronization during MVC compared with cramp, or smaller units than motor units are active, indicating that cramp is initiated close to or even at the muscle fiber level. Further research is needed to draw final conclusions.     

A simulation study to examine the use of cross-correlation as an estimate of surface EMG cross talk.

Cross-correlation between surface electromyogram (EMG) signals is commonly used as a means of quantifying EMG cross talk during voluntary activation. To examine the reliability of this method, the relationship between cross talk and the cross-correlation between surface EMG signals was examined by using model simulation. The simulation results illustrate an increase in cross talk with increasing subcutaneous fat thickness. The results also indicate that the cross-correlation function decays more rapidly with increasing distance from the active fibers than cross talk, which was defined as the normalized EMG amplitude during activation of a single muscle. The influence of common drive and short-term motor unit synchronization on the cross-correlation between surface EMG signals was also examined. While common drive did not alter the maximum value of the cross-correlation function, the correlation increased with increasing motor unit synchronization. It is concluded that cross-correlation analysis is not a suitable means of quantifying cross talk or of distinguishing between cross talk and coactivation during voluntary contraction. Furthermore, it is possible that a high correlation between surface EMG signals may reflect an association between motor unit firing times, for example due to motor unit synchronization.     

Dual task-related changes in the synchronous activity of wrist extensor type-identified motor units in humans

The coupling between the firings of 33 pairs of motor units tested in the extensor carpi radialis muscles was evaluated by cross-correlation analysis and compared during isometric wrist extension and hand clenching. A slightly greater amount of synchrony was observed during hand clenching (0.042 &#45 0.024 vs 0.035 &#45 0.017 synchronous impulses per trigger). This trend did not reach however the level of significance and the changes were actually found to be heterogeneous: in 15 out of the 33 pairs tested, synchronous activity with a narrow coupling (4.6 &#45 2.4 ms) consistent with short-term synchrony was greater during hand clenching whereas in nine other pairs, synchronous activity with a broader dispersion (9.0 &#45 4.5 ms) was reduced. These opposite changes could not be explained in terms of changes in the firing pattern of the motor units and were found instead to correlate with the motor units' biomechanical properties. Motor units with high recruitment thresholds and fast rising twitches showed predominantly an increase in synchrony; whereas the motor unit pairs with low recruitment thresholds and slow twitches showed either an increase or a decrease. The enhanced short-term synchrony suggests that common inputs distributed to motoneurones of all types were more effective during hand clenching whereas the decrease in weakly coupled synchronous activity suggests that other inputs synchronized at a pre-synaptic level and distributed more specifically to motor units recruited at low force levels were less effective. The possible origins of the inputs reflected in the dual changes are discussed in terms of the supra-spinal and peripheral pathways controlling the wrist extensor motoneurones during wrist extension and hand clenching.     

Dual task-related changes in the synchronous activity of wrist extensor type-identified motor units in humans

The coupling between the firings of 33 pairs of motor units tested in the extensor carpi radialis muscles was evaluated by cross-correlation analysis and compared during isometric wrist extension and hand clenching. A slightly greater amount of synchrony was observed during hand clenching (0.042 +/- 0.024 vs 0.035 +/- 0.017 synchronous impulses per trigger). This trend did not reach however the level of significance and the changes were actually found to be heterogeneous: in 15 out of the 33 pairs tested, synchronous activity with a narrow coupling (4.6 +/- 2.4 ms) consistent with short-term synchrony was greater during hand clenching whereas in nine other pairs, synchronous activity with a broader dispersion (9.0 +/- 4.5 ms) was reduced. These opposite changes could not be explained in terms of changes in the firing pattern of the motor units and were found instead to correlate with the motor units' biomechanical properties. Motor units with high recruitment thresholds and fast rising twitches showed predominantly an increase in synchrony; whereas the motor unit pairs with low recruitment thresholds and slow twitches showed either an increase or a decrease. The enhanced short-term synchrony suggests that common inputs distributed to motoneurones of all types were more effective during hand clenching whereas the decrease in weakly coupled synchronous activity suggests that other inputs synchronized at a pre-synaptic level and distributed more specifically to motor units recruited at low force levels were less effective. The possible origins of the inputs reflected in the dual changes are discussed in terms of the supra-spinal and peripheral pathways controlling the wrist extensor motoneurones during wrist extension and hand clenching.     

Effect of the tendon reflex on the silent period of motor units in man

The behavior of motor units functioning under different conditions was investigated during the patellar reflex. The reflex was elicited during regular firing of the motor units in connection with weak sustained voluntary effort without postural change. Under these conditions the firing rate of the motor units serves as a statistical characteristic of threshold: during the maintenance of an assigned level of contraction the mean firing rate of the low-threshold motor units was higher. The greater the mean spontaneous interspike interval of the motor units, the longer the duration of their silent period after reflex muscular contraction. The duration of the silent period of single motor units in many cases exceeded the longest duration of the aggregated silent period on the electromyogram. The instant frequency (the difference between the reciprocals of the mean interspike interval and silent period) was used as a measure of inhibitory action on the motoneuron. Positive correlation was observed between the change in the instant frequency and the spontaneous firing rate of the motor units. Within the population examined, those motoneurons whose frequency was higher (low-threshold) were more inhibited. The combination of spinal factors evoking inhibition of the motoneurons after the tendon reflex and the excitatory supraspinal influences causing recruiting of the motoneurons during voluntary contraction proved more effective under the conditions investigated for the same motoneurons.     

Factors Influencing the Estimates of Correlation between Motor Unit Activities in Humans

Background

Alpha motoneurons receive common synaptic inputs from spinal and supraspinal pathways. As a result, a certain degree of correlation can be observed between motoneuron spike trains during voluntary contractions. This has been studied by using correlation measures in the time and frequency domains. These measures are interpreted as reflecting different types of connectivity in the spinal networks, although the relation between the degree of correlation of the output motoneuron spike trains and of their synaptic inputs is unclear.

Methodology/Principal Findings

In this study, we analyze theoretically this relation and we complete this analysis by simulations and experimental data on the abductor digiti minimi muscle. The results demonstrate that correlation measures between motoneuron output spike trains are inherently influenced by the discharge rate and that this influence cannot be compensated by normalization. Because of the influence of discharge rate, frequency domain measures of correlation (coherence) do not identify the full frequency content of the common input signal when computed from pairs of motoneurons. Rather, an increase in sampling rate is needed by using cumulative spike trains of several motoneurons. Moreover, the application of averaging filters to the spike trains influences the magnitude of the estimated correlation levels calculated in the time, but not in the frequency domain (coherence).

Conclusions

It is concluded that the analysis of coherence in different frequency bands between cumulative spike trains of a sufficient number of motoneurons provides information on the spectrum of the common synaptic input. Nonetheless, the absolute values of coherent peaks cannot be compared across conditions with different cumulative discharge rates.     

Identification of alpha and gamma trigeminal motoneurons by the vibratome paraplast technique for HRP histochemistry

A morphometric analysis of the masseteric motoneuron pool of the trigeminal motor nucleus was performed in the rat using horseradish peroxidase as a marker. Thick (40 microns) cryosections and thin (7 microns) Paraplast sections were compared. Two types of motoneurons related to the masseter muscle were observed. Small motoneurons, which had a high nuclear index, were found interspersed between large motoneurons, which had more cytoplasm. Evidence is provided that the small trigeminal motoneurons are gamma neurons that innervate the intrafusal muscle fibers of the masseteric muscle spindles.     

Premotor interneurons in generation of adaptive leg reflexes and voluntary movements in stick insects

We investigated the role of local nonspiking interneurons involved in motor control of legs in the stick insect, Carausius morosus. In a preparation that allowed the animals to perform active leg movements such as adaptive tactile reflexes, proprioceptive reflexes, and walking, we gathered the following results. Almost all tested nonspiking interneurons that provide synaptic drive onto motoneurons of the proximal leg muscles contribute to all of the motor programs underlying tactile reflexes and voluntary leg movements such as walking, searching, and rocking. Most of them are also involved in the generation of proprioceptive reflexes. All motor programs for coactivation, avoidance reflexes, resistance reflexes, and voluntary leg movements result from parallel pathways including nonspiking interneurons that support and others that oppose the motoneuronal activity. The contribution of a single interneuron to the different motor programs is specific: it can be supporting for one motor program but opposing for the other. Even for the same motor program, for example, coactivation, the contribution of an individual interneuron can depend on the stimulus site from where the response is elicited. Our results support the idea that the different motor patterns for adaptive tactile reflexes, resistance reflexes, and voluntary leg movements emerge from a multifunctional neuronal circuit that is reorganized corresponding to the motor behavior performed. The actual motor pattern is then shaped by distributed information processing in parallel supporting and opposing pathways. © 1996 John Wiley & Sons, Inc.