Estimates of persistent inward currents in tibialis anterior motor units during standing ramped contraction tasks in humans

Author(s):  
Obaid U Khurram ◽  
Francesco Negro ◽  
CJ Heckman ◽  
Christopher K. Thompson

Persistent inward currents (PICs) play an essential role in setting motor neuron gain and shaping motor unit firing patterns. Estimates of PICs in humans can be made using the paired motor unit analysis technique, which quantifies the difference in discharge rate of a lower-threshold motor unit at the recruitment onset and offset of a higher-threshold motor unit (∆F). Because PICs are highly dependent on the level of neuromodulatory drive, ∆F represents an estimate of level of neuromodulation at the level of the spinal cord. Most of the estimates of ∆F are performed under constrained, isometric, seated conditions. In the present study, we used high-density surface EMG arrays to discriminate motor unit firing patterns during isometric seated conditions with torque or EMG visual feedback and during unconstrained standing anterior-to-posterior movements with RMS EMG visual feedback. We were able to apply the paired motor unit analysis technique to the decomposed motor units in each of the three conditions. We hypothesized that ∆F would be higher during unconstrained standing anterior-to-posterior movements compared to the seated conditions, reflecting an increase in the synaptic input to MNs drive while standing. In agreement with previous work, we found that there was no evidence of a difference in ∆F between the seated and standing postures, although slight differences in the initial and peak discharge rates were observed. Taken together, our results suggest that both the standing and seated postures are likely not sufficiently different--both being "upright" postures--to result in large changes in neuromodulatory drive.

2020 ◽  
Author(s):  
Lucas B. R Orssatto ◽  
Karen Mackay ◽  
Anthony J Shield ◽  
Raphael L. Sakugawa ◽  
Anthony J. Blazevich ◽  
...  

This study tested the hypothesis that estimates of persistent inward currents (PICs) in the human plantar flexors would increase with the level of voluntary drive. Twenty-one participants volunteered for this study (29.2±2.6 years). High-density surface electromyograms were collected from soleus and gastrocnemius medialis during ramp-shaped isometric contractions to 10%, 20%, and 30% (torque rise of 2%/s and 30-s duration) of each participant's maximal torque. Motor units identified in all the contraction intensities were included in the paired-motor unit analysis to calculate delta frequency (ΔF) and estimate the PICs. Increases in PICs were observed from 10% to 20% (Δ=0.6 pps; p<0.001) and 20% to 30% (Δ=0.5 pps; p<0.001) in soleus, and from 10% to 20% (Δ=1.2 pps; p<0.001) but not 20% to 30% (Δ=0.09 pps; p=0.724) in gastrocnemius medialis. Maximal discharge rate increased for soleus and gastrocnemius medialis from 10% to 20% (respectively, Δ=1.75 pps, p<0.001; and Δ=2.43 pps, p<0.001) and 20% to 30% (respectively, Δ=0.80 pps, p<0.017; and Δ=0.92 pps, p=002). The repeated-measures correlation identified associations between ΔF and increases in maximal discharge rate for both soleus (r=0.64; p<0.001) and gastrocnemius medialis (r=0.77; p<0.001). An increase in voluntary drive tends to increase PIC strength, which has key implications for the control of force but also for comparisons between muscles or between studies when relative force levels might be different. These data indicate that increases in voluntary descending drive amplify PICs in humans and provide an important spinal mechanism for motor unit firing, and thus force output modulation.


Author(s):  
Lucas B R Orssatto ◽  
Karen Mackay ◽  
Anthony James Shield ◽  
Raphael Luiz Sakugawa ◽  
Anthony John Blazevich ◽  
...  

This study tested if estimates of persistent inward currents (PICs) in the plantar flexors would increase with the level of voluntary drive. High-density surface electromyograms were collected from soleus and gastrocnemius medialis of 21 participants during ramp-shaped isometric contractions to 10%, 20%, and 30% (torque rise and decline of 2%/s and 30-s duration) of each participant's maximal torque. Motor units identified in all the contraction intensities were included in the paired-motor unit analysis to calculate delta frequency (ΔF) and estimate the PICs. ΔF is the difference in discharge rate of the control unit at the time of recruitment and de-recruitment of the test unit. Increases in PICs were observed from 10% to 20% (Δ=0.6 pulse-per-second, pps; p<0.001) and 20% to 30% (Δ=0.5pps; p<0.001) in soleus, and from 10% to 20% (Δ=1.2pps; p<0.001) but not 20% to 30% (Δ=0.09pps; p=0.724) in gastrocnemius medialis. Maximal discharge rate increased for soleus and gastrocnemius medialis from 10% to 20% (respectively, Δ=1.75pps, p<0.001; and Δ=2.43pps, p<0.001) and 20% to 30% (respectively, Δ=0.80pps, p<0.017; and Δ=0.92pps, p=002). The repeated-measures correlation identified associations between ΔF and increases in maximal discharge rate for soleus (r=0.64; p<0.001) and gastrocnemius medialis (r=0.77; p<0.001). An increase in voluntary drive tends to increase PIC strength, which has key implications for the control of force but also for comparisons between muscles or studies when relative force levels are different. Increases in voluntary descending drive amplify PICs in humans and provide an important spinal mechanism for motor unit discharging, and thus force output modulation.


2018 ◽  
Vol 124 (6) ◽  
pp. 1438-1446 ◽  
Author(s):  
Yi-Ling Peng ◽  
Matthew S. Tenan ◽  
Lisa Griffin

Weakness of the vastus medialis oblique (VMO) has been proposed to explain the high prevalence of knee pain in female subjects. Clinicians commonly use exercises in an attempt to preferentially activate the VMO. Recently, our group found evidence to support clinical theory that the VMO is neurologically distinct from the vastus medialis (VM). However, the ability to voluntarily activate these muscle subsections is still disputed. The aim of this study was to determine if VM and VMO activation varies between sexes and if control of the two muscles is different between rehabilitation exercises. Thirteen men and 13 women performed isometric straight leg raises in two hip positions, neutral hip rotation and 30 degrees lateral hip rotation. Bipolar intramuscular fine-wire electrodes were inserted into the VM and VMO to obtain motor unit recruitment thresholds and initial firing rates at recruitment. Linear mixed models and Tukey post hoc tests were used to assess significant differences in 654 motor units. Women demonstrated faster motor unit firing rate at recruitment, 1.18 ± 0.56 Hz higher than men. Motor units fired 0.47 ± 0.19 Hz faster during neutral hip rotation compared with lateral hip rotation. The VMO motor units were recruited 2.92 ± 1.28% earlier than the VM. All motor units were recruited 3.74 ± 1.27% earlier during neutral hip rotation than lateral hip rotation. Thus the VM and the VMO can be activated differentially, and their motor unit recruitment properties are affected by sex and hip position. NEW & NOTEWORTHY This is the first study to reveal differential activation of the vastus medialis oblique from the vastus medialis in clinical exercise protocols. Our research group used fine-wire electrodes to examine EMG signals of the vastus medialis oblique and vastus medialis to avoid possible cross talk. We also consider the effect of sex on motor unit firing patterns because of higher prevalence of knee pain in women, and yet few studies evaluating the sex differences in neuromuscular control.


2019 ◽  
Author(s):  
Altamash Hassan ◽  
Christopher K. Thompson ◽  
Francesco Negro ◽  
Mark Cummings ◽  
Randy Powers ◽  
...  

AbstractThe nervous system has a tremendous ability to modify motoneuron excitability according to task demands through neuromodulatory synaptic input to motoneurons. Neuromodulatory inputs adjust the response of the motoneuron to excitatory and inhibitory ionotropic input and can facilitate the induction of persistent inward currents (PICs). PICs amplify and prolong the motoneuron response to synaptic inputs, and PIC impairment may play a major role in motor deficits observed in pathological conditions. Noninvasive estimation of the magnitude of neuromodulatory input and persistent inward currents in human motoneurons is achieved through a paired motor unit analysis (ΔF) that quantifies hysteresis in the firing rates at motor unit recruitment and derecruitment. While the ΔF technique is commonly used for estimating motoneuron excitability, computational parameters used for the technique vary across studies. In the present study, we assessed the sensitivity of the ΔF technique to several criteria commonly used in selecting motor unit pairs for analysis, as well as to methods used for smoothing the instantaneous motor unit firing rates. Using HD-sEMG and motor unit decomposition we obtained 5,409 motor unit pairs from the triceps brachii of ten healthy individuals during submaximal triangle contractions. The mean (SD) ΔF was 4.9 (1.08) pps, consistent with previous work using intramuscular recordings. There was an exponential plateau relationship between ΔF and the recruitment time difference between the motor unit pairs, with the plateau occurring at approximately 1 s. There was an exponential decay relationship between ΔF and the derecruitment time difference between the motor unit pairs, with the decay stabilizing at approximately 1.5 s. We found that reducing or removing the minimum threshold for the correlation of the rate-rate slope for the two units did not affect ΔF values or variance. Additionally, we found that removing motor unit pairs in which the control unit was saturated had no significant effect on ΔF. Smoothing filter selection had no substantial effect on ΔF values and ΔF variance; however, the length and type of smoothing filter affected the minimum recruitment and derecruitment time differences. Our results facilitate interpretation of findings from studies that implement the ΔF approach but use different computational parameters.


2009 ◽  
Vol 102 (4) ◽  
pp. 2265-2272 ◽  
Author(s):  
Parveen Bawa ◽  
Chantelle Murnaghan

The phenomena of substitution and rotation among motor units of a muscle were examined in seven different muscles. Intramuscular motor unit activity and surface electromyographic (EMG) activity were recorded from one of the following muscles: abductor digiti minimi, first dorsal interosseous, extensor digitorum communis, flexor and extensor carpi radialis, tibialis anterior, and soleus. The subject was asked to discharge a discernible unit at a comfortable constant or rhythmically (pseudosinusoidally) modulated rate with audio and visual feedback. Results are reported from a total of 42 sets of motor units from all seven muscles. We observed that when a subject fired a motor unit for a long period, an additional motor unit frequently started to discharge after a few minutes. When the subject was asked to keep activity down to one unit, very often it was Unit 1 that dropped and Unit 2 continued to fire. Whereas Unit 2 had fired for a few minutes, Unit 1 resumed firing without any conscious effort by the subject. If the subject was then asked to retain just one unit, it was Unit 2 that dropped. Rhythmic modulation of firing rate of a tonically firing unit showed that whereas the threshold of this unit increased, the threshold of a phasically discharging unit decreased substantially. The increase in threshold of a tonically discharging unit is suggested to arise from inactivation of Na+ and Ca2+ channels and the decrease in threshold of higher-threshold units is suggested to arise from an increase in persistent inward currents that may occur during prolonged contractions. Whether a unit stops or starts to fire is suggested to depend on a balance between the strength of the central motor command, persistent inward currents, and inactivation of voltage-gated channels. Such rotations among low-threshold motoneurons would ensure low-level sustained contractions to be viable not only in small hand muscles but also in larger limb muscles.


Author(s):  
Alexander M. Zero ◽  
Eric A. Kirk ◽  
Charles L. Rice

During activity-dependent potentiation (ADP) motor unit firing rates (MUFRs) are lower, however, the mechanism for this response is not known. During increasing torque isometric contractions at low contraction intensities, MUFR trajectories initially accelerate and saturate demonstrating a non-linear response due to the activation of persistent inward currents (PICs) at the motoneuron. The purpose was to assess whether PICs are a factor in the reduction of MUFRs during ADP. To assess this, MUFR trajectories were fit with competing functions of linear regression and a rising exponential (i.e., acceleration and saturation). Using fine-wire electrodes, discrete MU potential trains were recorded in the tibialis anterior during slowly increasing dorsiflexion contractions to 10% of maximal voluntary contraction following both voluntary (post-activation potentiation; PAP) and evoked (post-tetanic potentiation; PTP) contractions. In 8 participants, 25 MUs were recorded across both ADP conditions and compared to the control with no ADP effect. During PAP and PTP, the average MUFRs were 16.4% and 9.2% lower (both P≤ 0.001), respectively. More MUFR trajectories were better fit to the rising exponential during control (16/25) compared to PAP (4/25, P<0.001) and PTP (8/25, P=0.03). The MU samples that had a rising exponential MUFR trajectory during PAP and PTP displayed an ~11% lower initial acceleration compared to control (P<0.05). Thus, synaptic amplification and MUFR saturation due to PIC properties are attenuated during ADP regardless of the type of conditioning contraction. This response may contribute to lower MUFRs and likely occurred because synaptic input is reduced when contractile function is enhanced.


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.


2020 ◽  
Vol 123 (6) ◽  
pp. 2209-2216 ◽  
Author(s):  
Jennifer M. Jakobi ◽  
Samantha L. Kuzyk ◽  
Chris J. McNeil ◽  
Brian H. Dalton ◽  
Geoffrey A. Power

Our findings indicate that lower electromyographic activity during the torque-enhanced condition following active lengthening compared with a purely isometric contraction arises from fewer active motor units and a lower discharge rate of those that are active. We used an acute condition of increased torque capacity to induce a decrease in net output of the motor neuron pool during a submaximal task to demonstrate, in humans, the impact of motor unit activity on torque steadiness.


2005 ◽  
Vol 94 (5) ◽  
pp. 3126-3133 ◽  
Author(s):  
Benjamin Pasquet ◽  
Alain Carpentier ◽  
Jacques Duchateau

This study examines the effect of fascicle length change on motor-unit recruitment and discharge rate in the human tibialis anterior (TA) during isometric contractions of various intensities. The torque produced during dorsiflexion and the surface and intramuscular electromyograms (EMGs) from the TA were recorded in eight subjects. The behavior of the same motor unit ( n = 59) was compared at two ankle joint angles (+10 and −10° around the ankle neutral position). Muscle fascicle length of the TA was measured noninvasively using ultrasonography recordings. When the ankle angle was moved from 10° plantarflexion to 10° dorsiflexion, the torque produced during maximal voluntary contraction (MVC) was significantly reduced [35.2 ± 3.3 vs. 44.3 ± 4.2 (SD) Nm; P < 0.001] and the average surface EMG increased (0.47 ± 0.08 vs. 0.43 ± 0.06 mV; P < 0.05). At reduced ankle joint angle, muscle fascicle length declined by 12.7% ( P < 0.01) at rest and by 18.9% ( P < 0.001) during MVC. Motor units were activated at a lower recruitment threshold for short compared with long muscle fascicle length, either when expressed in absolute values (2.1 ± 2.5 vs. 3.6 ± 3.7 Nm; P < 0.001) or relative to their respective MVC (5.2 ± 6.1 vs. 8.8 ± 9.0%). Higher discharge rate and additional motor-unit recruitment were observed at a given absolute or relative torque when muscle fascicles were shortened. However, the data indicate that increased rate coding was mainly present at low torque level (<10% MVC), when the muscle-tendon complex was compliant, whereas recruitment of additional motor units played a dominant role at higher torque level and decreased compliance (10–35% MVC). Taken together, the results suggest that the central command is modulated by the afferent proprioceptive information during submaximal contractions performed at different muscle fascicle lengths.


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