scholarly journals Spinal motoneurons of the human newborn are highly synchronized during leg movements

2020 ◽  
Vol 6 (47) ◽  
pp. eabc3916 ◽  
Author(s):  
A. Del Vecchio ◽  
F. Sylos-Labini ◽  
V. Mondì ◽  
P. Paolillo ◽  
Y. Ivanenko ◽  
...  

Motoneurons of neonatal rodents show synchronous activity that modulates the development of the neuromuscular system. However, the characteristics of the activity of human neonatal motoneurons are largely unknown. Using a noninvasive neural interface, we identified the discharge timings of individual spinal motoneurons in human newborns. We found highly synchronized activities of motoneurons of the tibialis anterior muscle, which were associated with fast leg movements. Although neonates’ motor units exhibited discharge rates similar to those of adults, their synchronization was significantly greater than in adults. Moreover, neonatal motor units showed coherent oscillations in the delta band, which is directly translated into force generation. These results suggest that motoneuron synchronization in human neonates might be an important mechanism for controlling fast limb movements, such as those of primitive reflexes. In addition to help revealing mechanisms of development, the proposed neural interface might monitor children at risk of developing motor disorders.

Author(s):  
Eduardo Martinez-Valdes ◽  
Francesco Negro ◽  
Michail Arvanitidis ◽  
Dario Farina ◽  
Deborah Falla

At high forces, the discharge rates of lower and higher threshold motor units (MU) are influenced in a different way by muscle pain. These differential effects may be particularly important for performing contractions at different speeds since the proportion of lower and higher threshold MUs recruited varies with contraction velocity. We investigated whether MU discharge and recruitment strategies are differentially affected by pain depending on their recruitment threshold (RT), across a range of contraction speeds. Participants performed ankle dorsiflexion sinusoidal-isometric contractions at two frequencies (0.25Hz and 1Hz) and two modulation amplitudes [5% and 10% of the maximum voluntary contraction (MVC)] with a mean target torque of 20%MVC. High-density surface electromyography recordings from the tibialis anterior muscle were decomposed and the same MUs were tracked across painful (hypertonic saline injection) and non-painful conditions. Torque variability, mean discharge rate (MDR), DR variability (DRvar), RT and the delay between the cumulative spike train and the resultant torque output (neuromechanical delay, NMD) were assessed. The average RT was greater at faster contraction velocities (p=0.01) but was not affected by pain. At the fastest contraction speed, torque variability and DRvar were reduced (p<0.05) and MDR was maintained. Conversely, MDR decreased and DRvar and NMD increased significantly during pain at slow contraction speeds (p<0.05). These results show that reductions in contraction amplitude and increased recruitment of higher threshold MUs at fast contraction speeds appears to compensate for the inhibitory effect of nociceptive inputs on lower threshold MUs, allowing the exertion of fast submaximal contractions during pain.


2019 ◽  
Vol 127 (4) ◽  
pp. 1034-1041
Author(s):  
Christopher K. Thompson ◽  
Michael D. Johnson ◽  
Francesco Negro ◽  
Laura Miller Mcpherson ◽  
Dario Farina ◽  
...  

The spontaneous or self-sustained discharge of spinal motoneurons can be observed in both animals and humans. Although the origins of this self-sustained discharge are not fully known, it can be generated by activation of persistent inward currents intrinsic to the motoneuron. If self-sustained discharge is generated exclusively through this intrinsic mechanism, the discharge of individual motor units will be relatively independent of one another. Alternatively, if increased activation of premotor circuits underlies this prolonged discharge of spinal motoneurons, we would expect correlated activity among motoneurons. Our aim is to assess potential synaptic drive by quantifying coherence during self-sustained discharge of spinal motoneurons. Electromyographic activity was collected from 20 decerebrate animals using a 64-channel electrode grid placed on the isolated soleus muscle before and following intrathecal administration of methoxamine, a selective α1-noradrenergic agonist. Sustained muscle activity was recorded and decomposed into the discharge times of ~10–30 concurrently active individual motor units. Consistent with previous reports, the self-sustained discharge of motor units occurred at low mean discharge rates with low-interspike variability. Before methoxamine administration, significant low-frequency coherence (<2 Hz) was observed, while minimal coherence was observed within higher frequency bands. Following intrathecal administration of methoxamine, increases in motor unit discharge rates and strong coherence in both the low-frequency and 15- to 30-Hz beta bands were observed. These data demonstrate beta-band coherence among motor units can be observed through noncortical mechanisms and that neuromodulation of spinal/brainstem neurons greatly influences coherent discharge within spinal motor pools. NEW & NOTEWORTHY The correlated discharge of spinal motoneurons is often used to describe the input to the motor pool. We demonstrate spinal/brainstem neurons devoid of cortical input can generate correlated motor unit discharge in the 15- to 30-Hz beta band, which is amplified through neuromodulation. Activity in the beta band is often ascribed to cortical drive in humans; however, these data demonstrate the capability of the mammalian segmental motor system to generate and modulate this coherent state of motor unit discharge.


2011 ◽  
Vol 106 (5) ◽  
pp. 2688-2697 ◽  
Author(s):  
Francesco Negro ◽  
Dario Farina

Oscillations in the primary motor cortex are transmitted through the corticospinal tract to the motoneuron pool. This pathway is believed to produce an effective and direct command from the motor cortex to the spinal motoneurons for the modulation of the force output. In this study, we used a computational model of a population of motoneurons to investigate the factors that can influence the transmission of the cortical input to the output of motoneurons, since it can be quantified by coherence analysis. The simulations demonstrated that, despite the nonlinearity of the motoneurons, oscillations present in the cortical input are transmitted to the output of the motoneuron pool at the same frequency. However, the interference introduced by the nonlinearity of the system increases the variability of the oscillations in output, introducing spectral lines whose frequency depends on the input frequencies and the motoneuron discharge rates. Moreover, an additional source of synaptic input common to all motoneurons but independent from the corticospinal component decorrelates the cortical input and motoneuron output and, thus, decreases the magnitude of the estimated coherence, even if the effective cortical drive does not change. These results indicate that the corticospinal input can effectively be sampled by a small population of motoneurons. However, the transmission of a corticospinal drive to the motoneuron pool is influenced by the nonlinearity of the spiking processes of the active motoneurons and by synaptic inputs common to the motoneuron population but independent from the cortical input.


2003 ◽  
Vol 95 (3) ◽  
pp. 1045-1054 ◽  
Author(s):  
C. J. Houtman ◽  
D. F. Stegeman ◽  
J. P. Van Dijk ◽  
M. J. Zwarts

To obtain more insight into the changes in mean muscle fiber conduction velocity (MFCV) during sustained isometric exercise at relatively low contraction levels, we performed an in-depth study of the human tibialis anterior muscle by using multichannel surface electromyogram. The results show an increase in MFCV after an initial decrease of MFCV at 30 or 40% maximum voluntary contraction in all of the five subjects studied. With a peak velocity analysis, we calculated the distribution of conduction velocities of action potentials in the bipolar electromyogram signal. It shows two populations of peak velocities occurring simultaneously halfway through the exercise. The MFCV pattern implies the recruitment of two different populations of motor units. Because of the lowering of MFCV of the first activated population of motor units, the newly recruited second population of motor units becomes visible. It is most likely that the MFCV pattern can be ascribed to the fatiguing of already recruited predominantly type I motor units, followed by the recruitment of fresh, predominantly type II, motor units.


2013 ◽  
Vol 109 (11) ◽  
pp. 2705-2711 ◽  
Author(s):  
M. Bączyk ◽  
A. Hałuszka ◽  
W. Mrówczyński ◽  
J. Celichowski ◽  
P. Krutki

The study aimed at determining the influence of a whole body vibration (WBV) on electrophysiological properties of spinal motoneurons. The WBV training was performed on adult male Wistar rats, 5 days a week, for 5 wk, and each daily session consisted of four 30-s runs of vibration at 50 Hz. Motoneuron properties were investigated intracellularly during experiments on deeply anesthetized animals. The experimental group subjected to the WBV consisted of seven rats, and the control group of nine rats. The WBV treatment induced no significant changes in the passive membrane properties of motoneurons. However, the WBV-evoked adaptations in excitability and firing properties were observed, and they were limited to fast-type motoneurons. A significant decrease in rheobase current and a decrease in the minimum and the maximum currents required to evoke steady-state firing in motoneurons were revealed. These changes resulted in a leftward shift of the frequency-current relationship, combined with an increase in slope of this curve. The functional relevance of the described adaptive changes is the ability of fast motoneurons of rats subjected to the WBV to produce series of action potentials at higher frequencies in a response to the same intensity of activation. Previous studies proved that WBV induces changes in the contractile parameters predominantly of fast motor units (MUs). The data obtained in our experiment shed a new light to possible explanation of these results, suggesting that neuronal factors also play a substantial role in MU adaptation.


2018 ◽  
Vol 120 (6) ◽  
pp. 3246-3256 ◽  
Author(s):  
Spencer A. Murphy ◽  
Francesco Negro ◽  
Dario Farina ◽  
Tanya Onushko ◽  
Matthew Durand ◽  
...  

Following stroke, hyperexcitable sensory pathways, such as the group III/IV afferents that are sensitive to ischemia, may inhibit paretic motor neurons during exercise. We quantified the effects of whole leg ischemia on paretic vastus lateralis motor unit firing rates during submaximal isometric contractions. Ten chronic stroke survivors (>1 yr poststroke) and 10 controls participated. During conditions of whole leg occlusion, the discharge timings of motor units were identified from decomposition of high-density surface electromyography signals during repeated submaximal knee extensor contractions. Quadriceps resting twitch responses and near-infrared spectroscopy measurements of oxygen saturation as an indirect measure of blood flow were made. There was a greater decrease in paretic motor unit discharge rates during the occlusion compared with the controls (average decrease for stroke and controls, 12.3 ± 10.0% and 0.1 ± 12.4%, respectively; P < 0.001). The motor unit recruitment thresholds did not change with the occlusion (stroke: without occlusion, 11.68 ± 5.83%MVC vs. with occlusion, 11.11 ± 5.26%MVC; control: 11.87 ± 5.63 vs. 11.28 ± 5.29%MVC). Resting twitch amplitudes declined similarly for both groups in response to whole leg occlusion (stroke: 29.16 ± 6.88 vs. 25.75 ± 6.78 Nm; control: 38.80 ± 13.23 vs 30.14 ± 9.64 Nm). Controls had a greater exponential decline (lower time constant) in oxygen saturation compared with the stroke group (stroke time constant, 22.90 ± 10.26 min vs. control time constant, 5.46 ± 4.09 min; P < 0.001). Ischemia of the muscle resulted in greater neural inhibition of paretic motor units compared with controls and may contribute to deficient muscle activation poststroke. NEW & NOTEWORTHY Hyperexcitable inhibitory sensory pathways sensitive to ischemia may play a role in deficient motor unit activation post stroke. Using high-density surface electromyography recordings to detect motor unit firing instances, we show that ischemia of the exercising muscle results in greater inhibition of paretic motor unit firing rates compared with controls. These findings are impactful to neurophysiologists and clinicians because they implicate a novel mechanism of force-generating impairment poststroke that likely exacerbates baseline weakness.


2002 ◽  
Vol 88 (1) ◽  
pp. 265-276 ◽  
Author(s):  
Anna M. Taylor ◽  
Julie W. Steege ◽  
Roger M. Enoka

The purpose of the study was to quantify the effect of motor-unit synchronization on the spike-triggered average forces of a population of motor units. Muscle force was simulated by defining mechanical and activation characteristics of the motor units, specifying motor neuron discharge times, and imposing various levels of motor-unit synchronization. The model comprised 120 motor units. Simulations were performed for motor units 5–120 to compare the spike-triggered average responses in the presence and absence of motor-unit synchronization with the motor-unit twitch characteristics defined in the model. To synchronize motor-unit activity, selected motor-unit discharge times were adjusted; this kept the number of action potentials constant across the three levels of synchrony for each motor unit. Because there was some overlap of motor-unit twitches even at minimal discharge rates, the simulations indicated that spike-triggered averaging underestimates the twitch force of all motor units and the contraction time of motor units with contraction times longer than 49 ms. Although motor-unit synchronization increased the estimated twitch force and decreased the estimated contraction time of all motor units, spike-triggered average force changed systematically with the level of synchrony in motor units 59–120 (upper 90% of the range of twitch forces). However, the reduction in contraction time was similar for moderate and high synchrony. In conclusion, spike-triggered averaging appears to provide a biased estimate of the distribution of twitch properties for a population of motor units because twitch fusion causes an underestimation of twitch force for slow units and motor-unit synchronization causes an overestimation of force for fast motor units.


2020 ◽  
Vol 123 (1) ◽  
pp. 149-157 ◽  
Author(s):  
Jakob L. Dideriksen ◽  
Alessandro Del Vecchio ◽  
Dario Farina

The ability to produce rapid forces requires quick motor unit recruitment, high motor unit discharge rates, and fast motor unit force twitches. The relative importance of these parameters for maximum rate of force development (RFD), however, is poorly understood. In this study, we systematically investigated these relationships using a computational model of motor unit pool activity and force. Across simulations, neural and muscular properties were systematically varied in experimentally observed ranges. Motor units were recruited over an interval starting from contraction onset (range: 22–233 ms). Upon recruitment, discharge rates declined from an initial rate (range: 89–212 pulses per second), with varying likelihood of doublet (interspike interval of 3 ms; range: 0–50%). Finally, muscular adaptations were modeled by changing average twitch contraction time (range: 42–78 ms). Spectral analysis showed that the effective neural drive to the simulated muscle had smaller bandwidths than the average motor unit twitch, indicating that the bandwidth of the motor output, and thus the capacity for explosive force, was limited mainly by neural properties. The simulated RFD increased by 1,050 ± 281% maximal voluntary contraction force per second from the longest to the shortest recruitment interval. This effect was more than fourfold higher than the effect of increasing the initial discharge rate, more than fivefold higher than the effect of increasing the chance of doublets, and more than sixfold higher than the effect of decreasing twitch contraction times. The simulated results suggest that the physiological variation of the rate by which motor units are recruited during ballistic contractions is the main determinant for the variability in RFD across individuals. NEW & NOTEWORTHY An important limitation of human performance is the ability to generate explosive movements by means of rapid development of muscle force. The physiological determinants of this ability, however, are poorly understood. In this study, we show using extensive simulations that the rate by which motor units are recruited is the main limiting factor for maximum rate of force development.


2009 ◽  
Vol 102 (3) ◽  
pp. 1890-1901 ◽  
Author(s):  
Marco A. Minetto ◽  
Aleš Holobar ◽  
Alberto Botter ◽  
Dario Farina

We analyzed individual motor units during electrically elicited cramp contractions with the aim of characterizing the variability and degree of common oscillations in their discharges. Intramuscular and surface electromyographic (EMG) signals were detected from the abductor hallucis muscle of 11 healthy subjects (age 27.0 ± 3.7 yr) during electrically elicited cramps. In all, 48 motor units were identified from the intramuscular EMG. These motor units were active for 23.6 ± 16.2 s, during which their average discharge rate was 14.5 ± 5.1 pulses/s (pps) and their minimum and maximum rates were, respectively, 6.0 ± 0.8 and 25.0 ± 8.0 pps ( P < 0.001). The coefficient of variation for the interspike interval (ISI) was 44.6 ± 9.7% and doublet discharges constituted 4.1 ± 4.7% of the total number of discharges. In 38 motor units, the SD of the ISI was positively correlated to the mean ISI ( R2 = 0.37, P < 0.05). The coherence spectrum between smoothed discharge rates of pairs of motor units showed one significant peak at 1.4 ± 0.4 Hz for 29 of the 96 motor unit pairs and two significant peaks at 1.3 ± 0.5 and 1.5 ± 0.5 Hz for 8 motor unit pairs. The cross-correlation function between pairs of discharge rates showed a significant peak (0.52 ± 0.11) in 26 motor unit pairs. In conclusion, motor units active during cramps showed a range of discharge rates similar to that observed during voluntary contractions but larger ISI variability, probably due to large synaptic noise. Moreover, the discharge rates of the active motor units showed common oscillations.


1998 ◽  
Vol 6 (2) ◽  
pp. 155-174 ◽  
Author(s):  
Rosemary White-Traut ◽  
Jean Powlesland ◽  
Deborah Gelhar ◽  
Robert Chatterton ◽  
Mariana Morris

Oxytocin’s (OT) role in the onset and maintenance of labor and in the letdown reflex is well known. OT also has been recognized as a neurotransmitter having functions in the central nervous system, including an influence on behavior (e.g., initiation of maternal behavior). This research was conducted to (1) evaluate whether human tactile contact in the human newborn would increase urine OT levels and alter infant behavioral state, and (2) determine the reliability of measuring OT in human infant urine. Although the data did not support the hypotheses, it was noted that OT levels, significantly decreased in infants who cried during the study period and that there was no correlation between infant’s chronologic age and OT levels. The findings illustrate several methodologic and measurement problems in the study of OT in human infants and that urine sampling in the neonate is not the most reliable method to evaluate change in OT levels. Some general issues concerning research with human infants also are discussed. Further research is recommended to document baseline levels of OT in neonates and to explore the use of salivary OT to measure short-term responses to interventions.


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