scholarly journals Sensitivity of the paired motor unit analysis for estimation of motoneuron excitability to commonly used constraints and filters

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.

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.


2017 ◽  
Vol 118 (1) ◽  
pp. 93-102 ◽  
Author(s):  
Seoan Huh ◽  
Ramamurthy Siripuram ◽  
Robert H. Lee ◽  
Vladimir V. Turkin ◽  
Derek O’Neill ◽  
...  

The majority of studies on the electrical properties of neurons are carried out in rodents, and in particular in mice. However, the minute size of this animal compared with humans potentially limits the relevance of the resulting insights. To be able to extrapolate results obtained in a small animal such as a rodent, one needs to have proper knowledge of the rules governing how electrical properties of neurons scale with the size of the animal. Generally speaking, electrical resistances of neurons increase as cell size decreases, and thus maintenance of equal depolarization across cells of different sizes requires the underlying currents to decrease in proportion to the size decrease. Thus it would generally be expected that voltage-sensitive currents are smaller in smaller animals. In this study, we used in vivo preparations to record electrical properties of spinal motoneurons in deeply anesthetized adult mice and cats. We found that PICs do not scale with size, but instead are constant in their amplitudes across these species. This constancy, coupled with the threefold differences in electrical resistances, means that PICs contribute a threefold larger depolarization in the mouse than in the cat. As a consequence, motoneuronal firing rate sharply increases as animal size decreases. These differences in firing rates are likely essential in allowing different species to control muscles with widely different contraction speeds (smaller animals have faster muscle fibers). Thus from our results we have identified a possible new mechanism for how electrical properties are tuned to match mechanical properties within the motor output system. NEW & NOTEWORTHY The small size of the mouse warrants concern over whether the properties of their neurons are a scaled version of those in larger animals or instead have unique features. Comparison of spinal motoneurons in mice to cats showed unique features. Firing rates in the mouse were much higher, in large part due to relatively larger persistent inward currents. These differences likely reflect adaptations for controlling much faster muscle fibers in mouse than cat.


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.


2020 ◽  
Vol 17 (1) ◽  
pp. 016063 ◽  
Author(s):  
Altamash Hassan ◽  
Christopher K Thompson ◽  
Francesco Negro ◽  
Mark Cummings ◽  
Randall K Powers ◽  
...  

2012 ◽  
Vol 107 (3) ◽  
pp. 808-823 ◽  
Author(s):  
Randall K. Powers ◽  
Sherif M. ElBasiouny ◽  
W. Zev Rymer ◽  
C. J. Heckman

Motoneuron discharge patterns reflect the interaction of synaptic inputs with intrinsic conductances. Recent work has focused on the contribution of conductances mediating persistent inward currents (PICs), which amplify and prolong the effects of synaptic inputs on motoneuron discharge. Certain features of human motor unit discharge are thought to reflect a relatively stereotyped activation of PICs by excitatory synaptic inputs; these features include rate saturation and de-recruitment at a lower level of net excitation than that required for recruitment. However, PIC activation is also influenced by the pattern and spatial distribution of inhibitory inputs that are activated concurrently with excitatory inputs. To estimate the potential contributions of PIC activation and synaptic input patterns to motor unit discharge patterns, we examined the responses of a set of cable motoneuron models to different patterns of excitatory and inhibitory inputs. The models were first tuned to approximate the current- and voltage-clamp responses of low- and medium-threshold spinal motoneurons studied in decerebrate cats and then driven with different patterns of excitatory and inhibitory inputs. The responses of the models to excitatory inputs reproduced a number of features of human motor unit discharge. However, the pattern of rate modulation was strongly influenced by the temporal and spatial pattern of concurrent inhibitory inputs. Thus, even though PIC activation is likely to exert a strong influence on firing rate modulation, PIC activation in combination with different patterns of excitatory and inhibitory synaptic inputs can produce a wide variety of motor unit discharge patterns.


2021 ◽  
Author(s):  
Altamash S Hassan ◽  
Melissa E Fajardo ◽  
Mark Cummings ◽  
Laura Miller McPherson ◽  
Francesco Negro ◽  
...  

Aging is a natural process that causes alterations in the neuromuscular system, which contribute to weakness and reduced quality of life. Reduced firing rates of individual motor units (MUs) likely contribute to weakness, but the mechanisms underlying reduced firing rates are not clear. Persistent inward currents (PICs) are crucial for the initiation, gain control, and maintenance of motoneuron firing, and are directly proportional to the level of monoaminergic input. Since the concentration of monoamines (i.e. serotonin and norepinephrine) are reduced with age, we sought to determine if estimates of PICs are reduced in older (>60 years old) compared to young adults (<35 years old). We decomposed MU spike trains from high-density surface electromyography over the biceps brachii and triceps brachii during isometric ramp contractions to 20% of maximum. Estimates of PICs (i.e. ΔF) were computed using the paired MU analysis technique. Regardless of the muscle, peak firing rates of older adults were reduced by ~1.6 pulses per second (pps) (P = 0.0292), and ΔF was reduced by ~1.9 pps (P < 0.0001), compared to young adults. We further found that age predicted ΔF in older adults (P = 0.0261), resulting in a reduction of ~1pps per decade, but there was no relationship in young adults (P = 0.9637). These findings suggest that PICs are reduced in older adults, and, further, age is a significant predictor of estimates of PICs in older adults. Reduced PIC magnitude represents one plausible mechanism for reduced firing rates and weakness in older individuals.


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):  
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.


2011 ◽  
Vol 106 (5) ◽  
pp. 2167-2179 ◽  
Author(s):  
Sharmila Venugopal ◽  
Thomas M. Hamm ◽  
Sharon M. Crook ◽  
Ranu Jung

Spasticity is commonly observed after chronic spinal cord injury (SCI) and many other central nervous system disorders (e.g., multiple sclerosis, stroke). SCI-induced spasticity has been associated with motoneuron hyperexcitability partly due to enhanced activation of intrinsic persistent inward currents (PICs). Disrupted spinal inhibitory mechanisms also have been implicated. Altered inhibition can result from complex changes in the strength, kinetics, and reversal potential ( ECl−) of γ-aminobutyric acid A (GABAA) and glycine receptor currents. Development of optimal therapeutic strategies requires an understanding of the impact of these interacting factors on motoneuron excitability. We employed computational methods to study the effects of conductance, kinetics, and ECl− of a dendritic inhibition on PIC activation and motoneuron discharge. A two-compartment motoneuron with enhanced PICs characteristic of SCI and receiving recurrent inhibition from Renshaw cells was utilized in these simulations. This dendritic inhibition regulated PIC onset and offset and exerted its strongest effects at motoneuron recruitment and in the secondary range of the current-frequency relationship during PIC activation. Increasing inhibitory conductance compensated for moderate depolarizing shifts in ECl− by limiting PIC activation and self-sustained firing. Furthermore, GABAA currents exerted greater control on PIC activation than glycinergic currents, an effect attributable to their slower kinetics. These results suggest that modulation of the strength and kinetics of GABAA currents could provide treatment strategies for uncontrollable spasms.


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