scholarly journals Low-frequency oscillations of the neural drive to the muscle are increased with experimental muscle pain

2012 ◽  
Vol 107 (3) ◽  
pp. 958-965 ◽  
Author(s):  
Dario Farina ◽  
Francesco Negro ◽  
Leonardo Gizzi ◽  
Deborah Falla

We investigated the influence of nociceptive stimulation on the accuracy of task execution and motor unit spike trains during low-force isometric contractions. Muscle pain was induced by infusion of hypertonic saline into the abductor digiti minimi muscle of 11 healthy men. Intramuscular EMG signals were recorded from the same muscle during four isometric contractions of 60-s duration at 10% of the maximal force [maximal voluntary contraction (MVC)] performed before injection (baseline), after injection of isotonic (control) or hypertonic saline (pain), and 15 min after pain was no longer reported. Each contraction was preceded by three 3-s ramp contractions from 0% to 10% MVC. The low-frequency oscillations of motor unit spike trains were analyzed by the first principal component of the low-pass filtered spike trains [first common component (FCC)], which represents the effective neural drive to the muscle. Pain decreased the accuracy of task performance [coefficient of variation (CoV) for force: baseline, 2.8 ± 1.8%, pain, 3.9 ± 1.8%; P < 0.05] and reduced motor unit discharge rates [11.6 ± 2.3 pulses per second (pps) vs. 10.7 ± 1.7 pps; P < 0.05]. Motor unit recruitment thresholds (2.2 ± 1.2% MVC vs. 2.4 ± 1.6% MVC), interspike interval variability (18.4 ± 4.9% vs. 19.1 ± 5.4%), strength of motor unit short-term synchronization [common input strength (CIS) 1.02 ± 0.44 vs. 0.83 ± 0.22], and strength of common drive (0.47 ± 0.08 vs. 0.47 ± 0.06) did not change across conditions. The FCC signal was correlated with force ( R = 0.45 ± 0.06), and the CoV for FCC increased in the painful condition (5.69 ± 1.29% vs. 7.83 ± 2.61%; P < 0.05). These results indicate that nociceptive stimulation increased the low-frequency variability in synaptic input to motoneurons.

2015 ◽  
Vol 113 (1) ◽  
pp. 182-191 ◽  
Author(s):  
Juan A. Gallego ◽  
Jakob L. Dideriksen ◽  
Ales Holobar ◽  
Jaime Ibáñez ◽  
José L. Pons ◽  
...  

Tremor in essential tremor (ET) is generated by pathological oscillations at 4–12 Hz, likely originating at cerebello-thalamo-cortical pathways. However, the way in which tremor is represented in the output of the spinal cord circuitries is largely unknown because of the difficulties in identifying the behavior of individual motor units from tremulous muscles. By using novel methods for the decomposition of multichannel surface EMG, we provide a systematic analysis of the discharge properties of motor units in nine ET patients, with concurrent recordings of EEG activity. This analysis allowed us to infer the contribution of common synaptic inputs to motor neurons in ET. Motor unit short-term synchronization was significantly greater in ET patients than in healthy subjects. Furthermore, the strong association between the degree of synchronization and the peak in coherence between motor unit spike trains at the tremor frequency indicated that the high synchronization levels were generated mainly by common synaptic inputs specifically at the tremor frequency. The coherence between EEG and motor unit spike trains demonstrated the presence of common cortical input to the motor neurons at the tremor frequency. Nonetheless, the strength of this input was uncorrelated to the net common synaptic input at the tremor frequency, suggesting a contribution of spinal afferents or secondary supraspinal pathways in projecting common input at the tremor frequency. These results provide the first systematic analysis of the neural drive to the muscle in ET and elucidate some of its characteristics that determine pathological tremulous muscle activity.


2012 ◽  
Vol 107 (12) ◽  
pp. 3357-3369 ◽  
Author(s):  
Jakob L. Dideriksen ◽  
Francesco Negro ◽  
Roger M. Enoka ◽  
Dario Farina

Motoneurons receive synaptic inputs from tens of thousands of connections that cause membrane potential to fluctuate continuously (synaptic noise), which introduces variability in discharge times of action potentials. We hypothesized that the influence of synaptic noise on force steadiness during voluntary contractions is limited to low muscle forces. The hypothesis was examined with an analytical description of transduction of motor unit spike trains into muscle force, a computational model of motor unit recruitment and rate coding, and experimental analysis of interspike interval variability during steady contractions with the abductor digiti minimi muscle. Simulations varied contraction force, level of synaptic noise, size of motor unit population, recruitment range, twitch contraction times, and level of motor unit short-term synchronization. Consistent with the analytical derivations, simulations and experimental data showed that force variability at target forces above a threshold was primarily due to low-frequency oscillations in neural drive, whereas the influence of synaptic noise was almost completely attenuated by two low-pass filters, one related to convolution of motoneuron spike trains with motor unit twitches (temporal summation) and the other attributable to summation of single motor unit forces (spatial summation). The threshold force above which synaptic noise ceased to influence force steadiness depended on recruitment range, size of motor unit population, and muscle contractile properties. This threshold was low (<10% of maximal force) for typical values of these parameters. Results indicate that motor unit recruitment and muscle properties of a typical muscle are tuned to limit the influence of synaptic noise on force steadiness to low forces and that the inability to produce a constant force during stronger contractions is mainly attributable to the common low-frequency oscillations in motoneuron discharge rates.


2020 ◽  
Vol 55 ◽  
pp. 101637 ◽  
Author(s):  
Chen Chen ◽  
Yang Yu ◽  
Shihan Ma ◽  
Xinjun Sheng ◽  
Chuang Lin ◽  
...  

2015 ◽  
Vol 114 (2) ◽  
pp. 1041-1047 ◽  
Author(s):  
Utku Ş. Yavuz ◽  
Francesco Negro ◽  
Deborah Falla ◽  
Dario Farina

It has been observed that muscle pain influences force variability and low-frequency (<3 Hz) oscillations in the neural drive to muscle. In this study, we aimed to investigate the effect of experimental muscle pain on the neural control of muscle force at higher frequency bands, associated with afferent feedback (alpha band, 5–13 Hz) and with descending cortical input (beta band, 15–30 Hz). Single-motor unit activity was recorded, in two separate experimental sessions, from the abductor digiti minimi (ADM) and tibialis anterior (TA) muscles with intramuscular wire electrodes, during isometric abductions of the fifth finger at 10% of maximal force [maximum voluntary contraction (MVC)] and ankle dorsiflexions at 25% MVC. The contractions were repeated under three conditions: no pain (baseline) and after intramuscular injection of isotonic (0.9%, control) and hypertonic (5.8%, painful) saline. The results showed an increase of the relative power of both the force signal and the neural drive at the tremor frequency band (alpha, 5–13 Hz) between the baseline and hypertonic (painful) conditions for both muscles ( P < 0.05) but no effect on the beta band. Additionally, the strength of motor unit coherence was lower ( P < 0.05) in the hypertonic condition in the alpha band for both muscles and in the beta band for the ADM. These results indicate that experimental muscle pain increases the amplitude of the tremor oscillations because of an increased variability of the neural control (common synaptic input) in the tremor band. Moreover, the concomitant decrease in coherence suggests an increase in independent input in the tremor band due to pain.


2006 ◽  
Vol 95 (5) ◽  
pp. 3245-3256 ◽  
Author(s):  
Michal Rivlin-Etzion ◽  
Ya'acov Ritov ◽  
Gali Heimer ◽  
Hagai Bergman ◽  
Izhar Bar-Gad

Spectral analysis of neuronal spike trains is an important tool in understanding the characteristics of neuronal activity by providing insights into normal and pathological periodic oscillatory phenomena. However, the refractory period creates high-frequency modulations in spike-train firing rate because any rise in the discharge rate causes a descent in subsequent time bins, leading to multifaceted modifications in the structure of the spectrum. Thus the power spectrum of the spiking activity (autospectrum) displays elevated energy in high frequencies relative to the lower frequencies. The spectral distortion is more dominant in neurons with high firing rates and long refractory periods and can lead to reduced identification of low-frequency oscillations (such as the 5- to 10-Hz burst oscillations typical of Parkinsonian basal ganglia and thalamus). We propose a compensation process that uses shuffling of interspike intervals (ISIs) for reliable identification of oscillations in the entire frequency range. This compensation is further improved by local shuffling, which preserves the slow changes in the discharge rate that may be lost in global shuffling. Cross-spectra of pairs of neurons are similarly distorted regardless of their correlation level. Consequently, identification of low-frequency synchronous oscillations, even for two neurons recorded by a single electrode, is improved by ISI shuffling. The ISI local shuffling is computed with confidence limits that are based on the first-order statistics of the spike trains, thus providing a reliable estimation of auto- and cross-spectra of spike trains and making it an optimal tool for physiological studies of oscillatory neuronal phenomena.


2021 ◽  
Author(s):  
François Hug ◽  
Simon Avrillon ◽  
Alessandro Del Vecchio ◽  
Andrea Casolo ◽  
Jaime Ibanez ◽  
...  

AbstractThere is a growing interest in decomposing high-density surface electromyography (HDsEMG) into motor unit spike trains to improve knowledge on the neural control of muscle contraction. However, the reliability of decomposition approaches is sometimes questioned, especially because they require manual editing of the outputs. We aimed to assess the inter-operator reliability of the identification of motor unit spike trains. Eight operators with varying experience in HDsEMG decomposition were provided with the same data extracted using the convolutive kernel compensation method. They were asked to manually edit them following established procedures. Data included signals from three lower leg muscles and different contraction intensities. After manual analysis, 126 ± 5 motor units were retained (range across operators: 119-134). A total of 3380 rate of agreement values were calculated (28 pairwise comparisons × 11 contractions/muscles × 4-28 motor units). The median rate of agreement value was 99.6%. Inter-operator reliability was excellent for both mean discharge rate and time at recruitment (intraclass correlation coefficient > 0.99). These results show that when provided with the same decomposed data and the same basic instructions, operators converge toward almost identical results. Our data have been made available so that they can be used for training new operators.


2004 ◽  
Vol 91 (3) ◽  
pp. 1250-1259 ◽  
Author(s):  
Dario Farina ◽  
Lars Arendt-Nielsen ◽  
Roberto Merletti ◽  
Thomas Graven-Nielsen

The aim of this human study was to investigate the relationship between experimentally induced muscle pain intensity (i.e., amount of nociceptive activity) and motor unit (MU) firing decrease and MU conduction velocity (CV). In 12 healthy subjects, nociceptive afferents were stimulated in the right tibialis anterior muscle by three intramuscular injections of hypertonic saline (0.2, 0.5, and 0.9 ml) separated by 140 s. The subjects performed six isometric contractions (20 s long) at 10% of the maximal voluntary contraction during the experimental muscle pain. The same set of six contractions was performed without any infusion before the painful condition on the right leg. The procedure was repeated for the left leg with infusion of isotonic (nonpainful) saline. Intramuscular and surface electromyographic (EMG) signals were collected to assess MU firing rate and CV. The firing rate of the active MUs [range: 7.4-14.8 pulses/s (pps)] did not change significantly in the three control conditions (without infusion for the right and left leg and with infusion of isotonic saline in the left leg). There was, on the contrary, a significant decrease (on average, mean ± SE, 1.03 ± 0.21 pps) of the firing rates during the painful condition. Moreover, MU firing rates were inversely significantly correlated with the subjective scores of pain intensity. Single MU CV was 3.88 ± 0.03 m/s (mean ± SE, over all the MUs) with no statistical difference among any condition, i.e., the injection of hypertonic saline did not alter the muscle fiber membrane properties of the observed MUs. Progressively increased muscle pain intensity causes a gradual decrease of MU firing rates. This decrease is not associated with a change in MU membrane properties, indirectly assessed by CV. This study demonstrates a central inhibitory motor control mechanism with an efficacy correlated to the nociceptive activity.


Author(s):  
Ales Holobar ◽  
Marco Alessandro Minetto ◽  
Alberto Botter ◽  
Francesco Negro ◽  
Dario Farina

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