Relationship Between Simulated Common Synaptic Input and Discharge Synchrony in Cat Spinal Motoneurons

2001 ◽  
Vol 86 (5) ◽  
pp. 2266-2275 ◽  
Author(s):  
Marc D. Binder ◽  
Randall K. Powers

Synchronized discharge of individual motor units is commonly observed in the muscles of human subjects performing voluntary contractions. The amount of this synchronization is thought to reflect the extent to which motoneurons in the same and related pools share common synaptic input. However, the relationship between the proportion of shared synaptic input and the strength of synchronization has never been measured directly. In this study, we simulated common shared synaptic input to cat spinal motoneurons by driving their discharge with noisy, injected current waveforms. Each motoneuron was stimulated with a number of different injected current waveforms, and a given pair of waveforms were either completely different or else shared a variable percentage of common elements. Cross-correlation histograms were then compiled between the discharge of motoneurons stimulated with noise waveforms with variable degrees of similarity. The strength of synchronization increased with the amount of simulated “common” input in a nonlinear fashion. Moreover, even when motoneurons had >90% of their simulated synaptic inputs in common, only ∼25–45% of their spikes were synchronized. We used a simple neuron model to explore how variations in neuron properties during repetitive discharge may lead to the low levels of synchronization we observed experimentally. We found that small variations in spike threshold and firing rate during repetitive discharge lead to large decreases in synchrony, particularly when neurons have a high degree of common input. Our results may aid in the interpretation of studies of motor unit synchrony in human hand muscles during voluntary contractions.

1993 ◽  
Vol 69 (4) ◽  
pp. 1005-1008 ◽  
Author(s):  
C. J. Heckman ◽  
M. D. Binder

1. As a human subject slowly increases the amount of force exerted by a muscle, the discharge rates of low-threshold motor units saturate at a rather low level, whereas higher-threshold units continue to be recruited and undergo increases in their discharge rates. The presently known intrinsic properties of motor units do not produce this "rate limiting." 2. Using computer simulations of a model motoneuron pool, we tested the hypothesis that rate limiting can be accounted for on the basis of the known distributions of synaptic input from different sources. The properties of the simulated motor units and their synaptic inputs were based as closely as possible on the available experimental data. A variety of simulated synaptic input organizations were applied to the pool, and the resulting outputs were compared with the data on rate limiting in human subjects. 3. We found that the data on rate limiting in human subjects greatly constrained the possible organizations of characterized synaptic input systems. Only when the synaptic organization included a gradual "crossover" between two specific types of input systems could the human data be accurately reproduced. Low input/output levels relied on a system organized like the monosynaptic Ia input, which produces greater effective synaptic currents in low- than in high-threshold motor units. Above a sharply defined crossover level, all further increases in output were produced by a system organized like the oligosynaptic rubrospinal input, which generates the opposite pattern.


1991 ◽  
Vol 71 (6) ◽  
pp. 2122-2126 ◽  
Author(s):  
D. J. Newham ◽  
T. McCarthy ◽  
J. Turner

The extent of voluntary activation in fresh and fatigued quadriceps muscles was investigated during isometric and isokinetic voluntary contractions at 20 and 150 degrees/s in 23 normal human subjects. The muscles were fatigued by a total of 4 min of maximal knee extension at an angular velocity of 85 degrees/s. Voluntary activation was determined by the superimposition of tetanic electrical stimulation at 100 Hz for 250 ms, initiated at a constant knee angle. The relationship between voluntary and stimulated force was similar to that found with the established twitch superimposition technique used on isometric contractions. In fresh muscle all the subjects showed full voluntary activation during isometric contractions. Some activation failure was seen in five subjects at 20 degrees/s [2.0 +/- 0.9 degrees (SE)] and in two subjects at 150 degrees/s (0.7 +/- 0.5). After fatigue all subjects showed some activation failure at 0 and 20 degrees/s (36.4 +/- 3.1 and 28.8 +/- 4.1 degrees, respectively), but only two showed any at 150 degrees/s (1.4 +/- 5.7). We conclude that brief high-intensity dynamic exercise can cause a considerable failure of voluntary activation. This failure was most marked during isometric and the lower-velocity isokinetic contractions. Thus a failure of voluntary activation may have greater functional significance than previous studies of isometric contractions have indicated.


2005 ◽  
Vol 94 (1) ◽  
pp. 206-218 ◽  
Author(s):  
Jamie A. Johnston ◽  
Sara A. Winges ◽  
Marco Santello

We recently examined the extent to which motor units of digit flexor muscles receive common input during multidigit grasping. This task elicited moderate to strong motor-unit synchrony (common input strength, CIS) across muscles (flexor digitorum profundus, FDP, and flexor pollicis longus, FPL) and across FDP muscle compartments, although the strength of this common input was not uniform across digit pairs. To further characterize the neural mechanisms underlying the control of multidigit grasping, we analyzed the relationship between firing of single motor units from these hand muscles in the frequency domain by computing coherence. We report three primary findings. First, in contrast to what has been reported in intrinsic hand muscles, motor units belonging to different muscles and muscle compartments of extrinsic digit flexors exhibited significant coherence in the 0- to 5- and 5- to 10-Hz frequency ranges and much weaker coherence in the higher 10–20 Hz range (maximum 0.0025 and 0.0008, respectively, pooled across all FDP compartment pairs). Second, the strength and incidence of coherence differed considerably across digit pairs. Third, contrary to what has been reported in the literature, across-muscle coherence can be stronger and more prevalent than within-muscle coherence, as FPL–FDP2 (thumb-index digit pair) exhibited the strongest and most prevalent coherence in our data (0.010 and 43% at 3 Hz, respectively). The heterogeneous organization of common input to these muscles and muscle compartments is discussed in relation to the functional role of individual digit pairs in the coordination of multiple digit forces in grasping.


2013 ◽  
Vol 110 (12) ◽  
pp. 2863-2872 ◽  
Author(s):  
Jessica M. D'Amico ◽  
Ş. Utku Yavuz ◽  
Ahmet Saraçoğlu ◽  
Elif Sibel Atiş ◽  
Monica A. Gorassini ◽  
...  

In animals, sodium- and calcium-mediated persistent inward currents (PICs), which produce long-lasting periods of depolarization under conditions of low synaptic drive, can be activated in trigeminal motoneurons following the application of the monoamine serotonin. Here we examined if PICs are activated in human trigeminal motoneurons during voluntary contractions and under physiological levels of monoaminergic drive (e.g., serotonin and norepinephrine) using a paired motor unit analysis technique. We also examined if PICs activated during voluntary contractions are larger in participants who demonstrate involuntary chewing during sleep (bruxism), which is accompanied by periods of high monoaminergic drive. In control participants, during a slowly increasing and then decreasing isometric contraction, the firing rate of an earlier-recruited masseter motor unit, which served as a measure of synaptic input to a later-recruited test unit, was consistently lower during derecruitment of the test unit compared with at recruitment (ΔF = 4.6 ± 1.5 imp/s). The ΔF, therefore, is a measure of the reduction in synaptic input needed to counteract the depolarization from the PIC to provide an indirect estimate of PIC amplitude. The range of ΔF values measured in the bruxer participants during similar voluntary contractions was the same as in controls, suggesting that abnormally high levels of monoaminergic drive are not continually present in the absence of involuntary motor activity. We also observed a consistent “onion skin effect” during the moderately sized contractions (<20% of maximal), whereby the firing rate of higher threshold motor units discharged at slower rates (by 4–7 imp/s) compared with motor units with relatively lower thresholds. The presence of lower firing rates in the more fatigue-prone, higher threshold trigeminal motoneurons, in addition to the activation of PICs, likely facilitates the activation of the masseter muscle during motor activities such as eating, nonnutritive chewing, clenching, and yawning.


Author(s):  
K. Kong ◽  
C. Ukachoke ◽  
G. McGuire ◽  
D. Wong ◽  
P. Ashby

AbstractBackgroundWe tested the effect of thiopental on the excitability of the corticospinal-motoneuron axis in normal human subjects.MethodsMagnetic stimulation was used to excite the neurons in the motor cortex which give rise to the fast conducting corticospinal pathway. The characteristics of the composite excitatory post-synaptic potentials (EPSPs) produced in individual spinal motoneurons by cortical stimulation were derived from changes in the firing probability of voluntarily activated motor units of the first dorsal interosseous muscle.ResultsIn 5 normal subjects, we found that thiopental, in incremental doses sufficient to sustain drowsiness (total dose 75 to 175 mg), significantly reduced the amplitude of these composite EPSPs.ConclusionsThiopental reduced the facilitation of motoneurons from the cortex most likely by depressing cortical neurons.


2015 ◽  
Vol 119 (11) ◽  
pp. 1337-1346 ◽  
Author(s):  
Anna Margherita Castronovo ◽  
Francesco Negro ◽  
Silvia Conforto ◽  
Dario Farina

α-Motor neurons receive synaptic inputs from spinal and supraspinal centers that comprise components either common to the motor neuron pool or independent. The input shared by motor neurons—common input—determines force control. The aim of the study was to investigate the changes in the strength of common synaptic input delivered to motor neurons with changes in force and with fatigue, two conditions that underlie an increase in the net excitatory drive to the motor neurons. High-density surface electromyogram (EMG) signals were recorded from the tibialis anterior muscle during contractions at 20, 50, and 75% of the maximal voluntary contraction force (in 3 sessions separated by at least 2 days), all sustained until task failure. EMG signal decomposition identified the activity of a total of 1,245 motor units. The coherence values between cumulative motor unit spike trains increased with increasing force, especially for low frequencies. This increase in coherence was not observed when comparing two subsets of motor units having different recruitment thresholds, but detected at the same force level. Moreover, the coherence values for frequencies <5 Hz increased at task failure with respect to the beginning of the contractions for all force levels. In conclusion, the results indicated that the relative strength of common synaptic input to motor neurons increases with respect to independent input when the net excitatory drive to motor neurons increases as a consequence of a change in force and fatigue.


1994 ◽  
Vol 19 (4) ◽  
pp. 451-461 ◽  
Author(s):  
Marc Heyters ◽  
Alain Carpentier ◽  
Jacques Duchateau ◽  
Karl Hainaut

The mechanical twitch in response to increasing electrical stimulus intensity, delivered both over the motor point and motor nerve, was recorded in the first dorsal interosseous (FDI) and the adductor pollicis (AP), and only over the motor point in the soleus (Sol), lateral (LG), and medial (MG) gastrocnemius muscles of human subjects. The relationship between intensity of electrical stimulation (ES) and twitch torque showed a positive linear regression in all muscles. In the FDI and AP the relationship was not significantly different when ES was applied at the motor point or over the motor nerve. At small intensities of activation, ES induced larger twitch torques in the MG and LG, which contain a roughly equal proportion of slow and fast motor units (MUs) compared to the Sol, which is composed mainly of slow type fibres. Moreover, the relationship between ES intensity and twitch time-to-peak is best fitted in all muscles by a power curve that shows a greater twitch time-to-peak range in its initial part for muscles containing a larger proportion of fast MUs (LG, MG) than for muscles mainly composed of slow MUs (Sol). In conclusion, these results induced by ES at the motor point and/or over the motor nerve confirm the concept of a reversed sequence of MU activation, as compared to voluntary contractions, and document this viewpoint in muscles of different function and composition. The reversed sequence of MU activation is more clearly evident during motor point ES. Key words: muscle contraction, mechanical twitch, motor point, nerve


2004 ◽  
Vol 92 (1) ◽  
pp. 523-535 ◽  
Author(s):  
Erica J. Weiss ◽  
Martha Flanders

Because humans have limited ability to independently control the many joints of the hand, a wide variety of hand shapes can be characterized as a weighted combination of just two or three main patterns of covariation in joint rotations, or “postural synergies.” The present study sought to align muscle synergies with these main postural synergies and to describe the form of membership of motor units in these postural/muscle synergies. Seventeen joint angles and the electromyographic (EMG) activities of several hand muscles (both intrinsic and extrinsic muscles) were recorded while human subjects held the hand statically in 52 specific shapes (i.e., shaping the hand around 26 commonly grasped objects or forming the 26 letter shapes of a manual alphabet). Principal-components analysis revealed several patterns of muscle synergy, some of which represented either coactivation of all hand muscles, or reciprocal patterns of activity (above and below average levels) in the intrinsic index finger and thumb muscles or (to a lesser extent) in the extrinsic four-tendoned extensor and flexor muscles. Single- and multiunit activity was generally a multimodal function of whole hand shape. This implies that motor-unit activation does not align with a single synergy; instead, motor units participate in multiple muscle synergies. Thus it appears that the organization of the global pattern of hand muscle activation is highly distributed. This organization mirrors the highly fractured somatotopy of cortical hand representations and may provide an ideal substrate for motor learning and recovery from injury.


2011 ◽  
Vol 106 (3) ◽  
pp. 1467-1479 ◽  
Author(s):  
Ann L. Revill ◽  
Andrew J. Fuglevand

Motor neurons are often assumed to generate spikes in proportion to the excitatory synaptic input received. There are, however, many intrinsic properties of motor neurons that might affect this relationship, such as persistent inward currents (PICs), spike-threshold accommodation, or spike-frequency adaptation. These nonlinear properties have been investigated in reduced animal preparation but have not been well studied during natural motor behaviors because of the difficulty in characterizing synaptic input in intact animals. Therefore, we studied the influence of each of these intrinsic properties on spiking responses and muscle force using a population model of motor units that simulates voluntary contractions in human subjects. In particular, we focused on the difference in firing rate of low-threshold motor units when higher threshold motor units were recruited and subsequently derecruited, referred to as ΔF. Others have used ΔF to evaluate the extent of PIC activation during voluntary behavior. Our results showed that positive ΔF values could arise when any one of these nonlinear properties was included in the simulations. Therefore, a positive ΔF should not be considered as exclusive evidence for PIC activation. Furthermore, by systematically varying contraction duration and speed in our simulations, we identified a means that might be used experimentally to distinguish among PICs, accommodation, and adaptation as contributors to ΔF.


2004 ◽  
Vol 91 (1) ◽  
pp. 57-62 ◽  
Author(s):  
Douglas A. Keen ◽  
Andrew J. Fuglevand

Short-term synchronization of active motor units has been attributed in part to last-order divergent projections that provide common synaptic input across motor neurons. The extent of synchrony thus allows insight as to how the inputs to motor neurons are distributed. Our particular interest relates to the organization of extrinsic finger muscles that give rise distally to multiple tendons, which insert onto all the fingers. For example, extensor digitorum (ED) is a multi-compartment muscle that extends digits 2–5. Given the unique architecture of ED, it is unclear if synaptic inputs are broadly distributed across the entire pool of motor neurons innervating ED or segregated to supply subsets of motor neurons innervating different compartments. Therefore the purpose of this study was to evaluate the degree of motor-unit synchrony both within and across compartments of ED. One hundred and forty-five different motor-unit pairs were recorded in the human ED of nine subjects during weak voluntary contractions. Cross-correlation histograms were generated for all of the motor-unit pairs and the degree of synchronization between two units was assessed using the index of common input strength (CIS). The degree of synchrony for motor-unit pairs within the same compartment (CIS = 0.7 ± 0.3; mean ± SD) was significantly greater than for motor-unit pairs in different compartments (CIS = 0.4 ± 0.22). Consequently, last-order synaptic projections are not distributed uniformly across the entire pool of motor neurons innervating ED but are segregated to supply subsets of motor neurons innervating different compartments.


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