scholarly journals Origins of Abnormal Excitability in Biceps Brachii Motoneurons of Spastic-Paretic Stroke Survivors

2009 ◽  
Vol 102 (4) ◽  
pp. 2026-2038 ◽  
Author(s):  
Carol J. Mottram ◽  
Nina L. Suresh ◽  
C. J. Heckman ◽  
Monica A. Gorassini ◽  
William Z. Rymer
Keyword(s):  
Motor Unit ◽  
Synaptic Input ◽  
Biceps Brachii ◽  
Motor Units ◽  
Lower Threshold ◽  
Spontaneous Discharge ◽  
Stroke Survivors ◽  
Test Unit ◽  
Threshold Test ◽  
Inward Currents

Stroke survivors often exhibit abnormal motoneuron excitability, manifested clinically as spasticity with exaggerated stretch reflexes in resting muscles. We examined whether this abnormal excitability is a result of increased activation of intrinsic voltage-dependent persistent inward currents (PICs) or whether it is a result of enhanced synaptic inputs to the motoneuron. This distinction was made by recording firing rate profiles of pairs of motor units during isometric contractions of elbow flexor muscles. To estimate PIC amplitude, the discharge of the lower-threshold (reporter) motor unit of the pair was used to estimate the synaptic input to the higher-threshold (test) motor unit. The estimated synaptic input required to recruit the test unit was compared with the synaptic input when the test unit was derecruited (Δ F) and this served as an estimate of the intrinsic (PIC) contribution to motoneuron firing. We found that PIC estimates were not larger in spastic-paretic motoneurons (Δ F = 4.0 ± 1.6 pps) compared with contralateral (4.6 ± 1.4 pps) and age-matched healthy control motoneurons (3.8 ± 1.7, all P > 0.1). Instead, following the voluntary contractions, the majority of lower-threshold motor units in spastic-paretic muscles (83%) exhibited spontaneous discharge, compared with 14% of contralateral and 0% of control motor units. Furthermore, there was strong co-modulation of simultaneously active units in spastic muscle. The presence of ongoing, correlated unit activity at “rest,” coupled with firing behavior at recruitment unique to lower-threshold motor units in spastic muscles, suggested that firing changes are likely a result of a low-level depolarizing synaptic drive to the resting motoneuron pool.

scholarly journals Amphetamine Increases Persistent Inward Currents in Human Motoneurons Estimated From Paired Motor-Unit Activity

2010 ◽  
Vol 103 (3) ◽  
pp. 1295-1303 ◽  
Author(s):  
Esther Udina ◽  
Jessica D'Amico ◽  
Austin J. Bergquist ◽  
Monica A. Gorassini
Keyword(s):  
Brain Stem ◽  
Motor Unit ◽  
Synaptic Input ◽  
Motor Units ◽  
Firing Frequency ◽  
Voluntary Contraction ◽  
Repetitive Firing ◽  
Test Unit ◽  
Threshold Control ◽  
Threshold Test

Recruitment and repetitive firing of spinal motoneurons depend on the activation of persistent inward calcium and sodium currents (PICs) that are in turn facilitated by serotonin and norepinephrine that arise primarily from the brain stem. Considering that in rats motoneuron PICs are greatly facilitated by increasing the presynaptic release of norepinephrine with amphetamine, we sought similar evidence for the modulation of PICs in human motoneurons. Pairs of motor units were recorded during a gradually increasing and then decreasing voluntary contraction. The firing frequency ( F) of the lower-threshold (control) motor unit was used as an estimate of the synaptic input to the higher-threshold (test) motor unit. Generally, PICs are initiated during the recruitment of a motoneuron and subsequently provide a fixed depolarizing current that helps the synaptic input maintain firing until derecruitment. Thus the amplitude of the PIC in the test motor unit was estimated from the difference in synaptic input (Δ F) needed to maintain minimal firing once the PIC was fully activated (measured at the time of test unit derecruitment) compared with the larger synaptic input required to initiate firing prior to full PIC activation (measured at the time of test unit recruitment; Δ F = Frecruit − Fderecruit). Moreover, the activation time of the PIC was estimated as the minimal contraction duration needed to produce a maximal PIC (Δ F). In five subjects, oral administration of amphetamine, but not placebo, increased the Δ F by 62% [from 3.7 ± 0.6 to 6.0 ± 0.8 (SD) imp/s, P = 0.001] and decreased the time needed to activate a maximal Δ F from ∼2 to 0.5 s. Both findings suggest that the endogenous facilitation of PICs from brain stem derived norepinephrine plays an important role in modulating human motoneuron excitability, readying motoneurons for rapid and sustained activity during periods of high arousal such as stress or fear.

scholarly journals Activation properties of trigeminal motoneurons in participants with and without bruxism

2013 ◽  
Vol 110 (12) ◽  
pp. 2863-2872 ◽  
Author(s):  
Jessica M. D'Amico ◽  
Ş. Utku Yavuz ◽  
Ahmet Saraçoğlu ◽  
Elif Sibel Atiş ◽  
Monica A. Gorassini ◽  
...  
Keyword(s):  
Firing Rate ◽  
Motor Unit ◽  
Synaptic Input ◽  
Motor Units ◽  
Sleep Bruxism ◽  
Test Unit ◽  
Motor Activities ◽  
Inward Currents ◽  
Trigeminal Motoneurons ◽  
Voluntary Contractions

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.

scholarly journals Origins of Spontaneous Firing of Motor Units in the Spastic–Paretic Biceps Brachii Muscle of Stroke Survivors

2010 ◽  
Vol 104 (6) ◽  
pp. 3168-3179 ◽  
Author(s):  
C. J. Mottram ◽  
C. L. Wallace ◽  
C. N. Chikando ◽  
W. Z. Rymer
Keyword(s):  
Motor Unit ◽  
Biceps Brachii ◽  
Motor Units ◽  
Afferent Feedback ◽  
Spontaneous Discharge ◽  
Stroke Survivors ◽  
Spontaneous Firing ◽  
Descending Pathways ◽  
Hemiparetic Stroke ◽  
Ramp Contractions

One potential expression of altered motoneuron excitability following a hemispheric stroke is the spontaneous unit firing (SUF) of motor units at rest. The elements contributing to this altered excitability could be spinal descending pathways, spinal interneuronal networks, afferent feedback, or intrinsic motoneuron properties. Our purpose was to examine the characteristics of spontaneous discharge in spastic–paretic and contralateral muscles of hemiparetic stroke survivors, to determine which of these mechanisms might contribute. To achieve this objective, we examined the statistics of spontaneous discharge of individual motor units and we conducted a coherence analyses on spontaneously firing motor unit pairs. The presence of significant coherence between units might indicate a common driving source of excitation to multiple motoneurons from descending pathways or regional interneurons, whereas a consistent lack of coherence might favor an intrinsic cellular mechanism of hyperexcitability. Spontaneous firing of motor units (i.e., ongoing discharge in the absence of an ongoing stimulus) was observed to a greater degree in spastic–paretic muscles (following 83.2 ± 16.7% of ramp contractions) than that in contralateral muscles (following just 14.1 ± 10.5% of ramp contractions; P < 0.001) and was not observed at all in healthy control muscle. The average firing rates of the spontaneously firing units were 8.4 ± 1.8 pulses/s (pps) in spastic–paretic muscle and 9.6 ± 2.2 pps in contralateral muscle ( P < 0.001). In 37 instances ( n = 63 pairs), we observed spontaneous discharge of two or more motor units simultaneously in spastic–paretic muscle. Seventy percent of the dually firing motor unit pairs exhibited significant coherence ( P < 0.001) in the 0- to 4-Hz bandwidth (average peak coherence: 0.14 ± 0.13; range: 0.01–0.75) and 22% of pairs exhibited significant coherence ( P < 0.001) in the 15- to 30-Hz bandwidth (average peak coherence: 0.07 ± 0.06; range: 0.01–0.31). We suggest that the spontaneous firing was likely not attributable solely to enhanced intrinsic motoneuron activation, but attributable, at least in part, to a low-level excitatory synaptic input to the resting spastic–paretic motoneuron pool, possibly from regional or supraspinal centers.

scholarly journals Disturbances of motor unit rate modulation are prevalent in muscles of spastic-paretic stroke survivors

2014 ◽  
Vol 111 (10) ◽  
pp. 2017-2028 ◽  
Author(s):  
C. J. Mottram ◽  
C. J. Heckman ◽  
R. K. Powers ◽  
W. Z. Rymer ◽  
N. L. Suresh
Keyword(s):  
Firing Rate ◽  
Motor Unit ◽  
Biceps Brachii ◽  
Lower Threshold ◽  
Stroke Survivors ◽  
Biceps Brachii Muscle ◽  
Firing Rates ◽  
Rate Modulation ◽  
Motor Unit Firing ◽  
And Control

Stroke survivors often exhibit abnormally low motor unit firing rates during voluntary muscle activation. Our purpose was to assess the prevalence of saturation in motor unit firing rates in the spastic-paretic biceps brachii muscle of stroke survivors. To achieve this objective, we recorded the incidence and duration of impaired lower- and higher-threshold motor unit firing rate modulation in spastic-paretic, contralateral, and healthy control muscle during increases in isometric force generated by the elbow flexor muscles. Impaired firing was considered to have occurred when firing rate became constant (i.e., saturated), despite increasing force. The duration of impaired firing rate modulation in the lower-threshold unit was longer for spastic-paretic (3.9 ± 2.2 s) than for contralateral (1.4 ± 0.9 s; P < 0.001) and control (1.1 ± 1.0 s; P = 0.005) muscles. The duration of impaired firing rate modulation in the higher-threshold unit was also longer for the spastic-paretic (1.7 ± 1.6 s) than contralateral (0.3 ± 0.3 s; P = 0.007) and control (0.1 ± 0.2 s; P = 0.009) muscles. This impaired firing rate of the lower-threshold unit arose, despite an increase in the overall descending command, as shown by the recruitment of the higher-threshold unit during the time that the lower-threshold unit was saturating, and by the continuous increase in averages of the rectified EMG of the biceps brachii muscle throughout the rising phase of the contraction. These results suggest that impairments in firing rate modulation are prevalent in motor units of spastic-paretic muscle, even when the overall descending command to the muscle is increasing.

Evidence for Plateau Potentials in Tail Motoneurons of Awake Chronic Spinal Rats With Spasticity

2001 ◽  
Vol 86 (4) ◽  
pp. 1972-1982 ◽  
Author(s):  
David J. Bennett ◽  
Yunru Li ◽  
Philip J. Harvey ◽  
Monica Gorassini
Keyword(s):  
Spinal Cord ◽  
Firing Rate ◽  
Motor Unit ◽  
Synaptic Input ◽  
Control Unit ◽  
Motor Units ◽  
Test Unit ◽  
Plateau Potentials ◽  
Motor Unit Firing ◽  
Chronic Spinal Rats

Motor units of segmental tail muscles were recorded in awake rats following acute (1–2 days) and chronic (>30 days) sacral spinal cord transection to determine whether plateau potentials contributed to sustained motor-unit discharges after injury. This study was motivated by a companion in vitro study that indicated that after chronic spinal cord injury, the tail motoneurons of the sacrocaudal spinal cord exhibit persistent inward currents ( I PIC) that cause intrinsically sustained depolarizations ( plateau potentials) and firing ( self-sustained firing). Importantly, in this companion study, the plateaus were fully activated at recruitment and subsequently helped sustain the firing without causing abrupt nonlinearities in firing. That is, after recruitment and plateau activation, the firing rate was modulated relatively linearly with injected current and therefore provided a good approximation of the input to the motoneuron despite the plateau. Thus in the present study, pairs of motor units were recorded simultaneously from the same muscle, and the firing rate ( F) of the lowest-threshold unit (control unit) was used as an estimate of the synaptic input to both units. We then examined whether firing of the higher-threshold unit (test unit) was intrinsically maintained by a plateau, by determining whether more synaptic input was required to recruit the test unit than to maintain its firing. The difference in the estimated synaptic input at recruitment and de-recruitment of the test unit (i.e., change in control unit rate, Δ F) was taken as an estimate of the plateau current ( I PIC) that intrinsically sustained the firing. Slowly graded manual skin stimulation was used to recruit and then de-recruit the units. The test unit was recruited when the control unit rate was on average 17.8 and 18.9 Hz in acute and chronic spinal rats, respectively. In chronic spinal rats, the test unit was de-recruited when the control unit rate (re: estimated synaptic input) was significantly reduced, compared with at recruitment (Δ F = −5.5 Hz), and thus a plateau participated in maintaining the firing. In the lowest-threshold motor units, even a brief stimulation triggered very long-lasting firing (seconds to hours; self-sustained firing). Higher-threshold units required continuous stimulation (or a spontaneous spasm) to cause firing, but again more synaptic input was needed to recruit the unit than to maintain its firing (i.e., plateau present). In contrast, in acute spinal rats, the stimulation did not usually trigger sustained motor-unit firing that could be attributed to plateaus because Δ F was not significantly different from zero. These results indicate that plateaus play an important role in sustaining motor-unit firing in awake chronic spinal rats and thus contribute to the hyperreflexia and hypertonus associated with chronic injury.

scholarly journals Preferential distribution of nociceptive input to motoneurons with muscle units in the cranial portion of the upper trapezius muscle

2016 ◽  
Vol 116 (2) ◽  
pp. 611-618 ◽  
Author(s):  
Jakob L. Dideriksen ◽  
Ales Holobar ◽  
Deborah Falla
Keyword(s):  
Motor Unit ◽  
Synaptic Input ◽  
Isotonic Saline ◽  
Trapezius Muscle ◽  
Motor Units ◽  
Noxious Stimulation ◽  
Caudal Region ◽  
Upper Trapezius ◽  
Upper Trapezius Muscle ◽  
Nociceptive Input

Pain is associated with changes in the neural drive to muscles. For the upper trapezius muscle, surface electromyography (EMG) recordings have indicated that acute noxious stimulation in either the cranial or the caudal region of the muscle leads to a relative decrease in muscle activity in the cranial region. It is, however, not known if this adaption reflects different recruitment thresholds of the upper trapezius motor units in the cranial and caudal region or a nonuniform nociceptive input to the motor units of both regions. This study investigated these potential mechanisms by direct motor unit identification. Motor unit activity was investigated with high-density surface EMG signals recorded from the upper trapezius muscle of 12 healthy volunteers during baseline, control (intramuscular injection of isotonic saline), and painful (hypertonic saline) conditions. The EMG was decomposed into individual motor unit spike trains. Motor unit discharge rates decreased significantly from control to pain conditions by 4.0 ± 3.6 pulses/s (pps) in the cranial region but not in the caudal region (1.4 ± 2.8 pps; not significant). These changes were compatible with variations in the synaptic input to the motoneurons of the two regions. These adjustments were observed, irrespective of the location of noxious stimulation. These results strongly indicate that the nociceptive synaptic input is distributed in a nonuniform way across regions of the upper trapezius muscle.

scholarly journals Common Synaptic Input to the Human Hypoglossal Motor Nucleus

2011 ◽  
Vol 105 (1) ◽  
pp. 380-387 ◽  
Author(s):  
Christopher M. Laine ◽  
E. Fiona Bailey
Keyword(s):  
Firing Rate ◽  
Motor Unit ◽  
Synaptic Input ◽  
Motor Units ◽  
Motor Nucleus ◽  
Tongue Protrusion ◽  
Ongoing Research ◽  
Airway Patency ◽  
Significant Difference ◽  
Common Drive

The tongue plays a key role in various volitional and automatic functions such as swallowing, maintenance of airway patency, and speech. Precisely how hypoglossal motor neurons, which control the tongue, receive and process their often concurrent input drives is a subject of ongoing research. We investigated common synaptic input to the hypoglossal motor nucleus by measuring the coordination of spike timing, firing rate, and oscillatory activity across motor units recorded from unilateral (i.e., within a belly) or bilateral (i.e., across both bellies) locations within the genioglossus (GG), the primary protruder muscle of the tongue. Simultaneously recorded pairs of motor units were obtained from 14 healthy adult volunteers using tungsten microelectrodes inserted percutaneously into the GG while the subjects were engaged in volitional tongue protrusion or rest breathing. Bilateral motor unit pairs showed concurrent low frequency alterations in firing rate (common drive) with no significant difference between tasks. Unilateral motor unit pairs showed significantly stronger common drive in the protrusion task compared with rest breathing, as well as higher indices of synchronous spiking (short-term synchrony). Common oscillatory input was assessed using coherence analysis and was observed in all conditions for frequencies up to ∼5 Hz. Coherence at frequencies up to ∼10 Hz was strongest in motor unit pairs recorded from the same GG belly in tongue protrusion. Taken together, our results suggest that cortical drive increases motor unit coordination within but not across GG bellies, while input drive during rest breathing is distributed uniformly to both bellies of the muscle.

scholarly journals Motor unit activity in biceps brachii of left-handed humans during sustained contractions with two load types

2016 ◽  
Vol 116 (3) ◽  
pp. 1358-1365 ◽  
Author(s):  
Jeffrey R. Gould ◽  
Brice T. Cleland ◽  
Diba Mani ◽  
Ioannis G. Amiridis ◽  
Roger M. Enoka
Keyword(s):  
Motor Unit ◽  
Unit Activity ◽  
Position Control ◽  
Biceps Brachii ◽  
Motor Units ◽  
Motor Unit Activity ◽  
Time Interaction ◽  
Left Handed ◽  
Position Task ◽  
Task Time

The purpose of the study was to compare the discharge characteristics of single motor units during sustained isometric contractions that required either force or position control in left-handed individuals. The target force for the two sustained contractions (24.9 ± 10.5% maximal force) was identical for each biceps brachii motor unit ( n = 32) and set at 4.7 ± 2.0% of maximal voluntary contraction (MVC) force above its recruitment threshold (range: 0.5–41.2% MVC force). The contractions were not sustained to task failure, but the duration (range: 60–330 s) was identical for each motor unit and the decline in MVC force immediately after the sustained contractions was similar for the two tasks (force: 11.1% ± 13.7%; position: 11.6% ± 9.9%). Despite a greater increase in the rating of perceived exertion during the position task (task × time interaction, P < 0.006), the amplitude of the surface-recorded electromyogram for the agonist and antagonist muscles increased similarly during the two tasks. Nonetheless, mean discharge rate of the biceps brachii motor units declined more during the position task (task × time interaction, P < 0.01) and the variability in discharge times (coefficient of variation for interspike interval) increased only during the position task (task × time interaction, P < 0.008). When combined with the results of an identical study on right-handers (Mottram CJ, Jakobi JM, Semmler JG, Enoka RM. J Neurophysiol 93: 1381–1392, 2005), the findings indicate that handedness does not influence the adjustments in biceps brachii motor unit activity during sustained submaximal contractions requiring either force or position control.

scholarly journals Influence of common synaptic input to motor neurons on the neural drive to muscle in essential tremor

2015 ◽  
Vol 113 (1) ◽  
pp. 182-191 ◽  
Author(s):  
Juan A. Gallego ◽  
Jakob L. Dideriksen ◽  
Ales Holobar ◽  
Jaime Ibáñez ◽  
José L. Pons ◽  
...  
Keyword(s):  
Motor Unit ◽  
Motor Neurons ◽  
Synaptic Input ◽  
Motor Units ◽  
Spike Trains ◽  
Neural Drive ◽  
Systematic Analysis ◽  
Synaptic Inputs ◽  
Tremor Frequency ◽  
Unit Spike

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.

scholarly journals Persistent Inward Currents Increase With The Level Of Voluntary Drive In Plantar Flexor Low-Threshold Motor Units

2020 ◽  
Author(s):  
Lucas B. R Orssatto ◽  
Karen Mackay ◽  
Anthony J Shield ◽  
Raphael L. Sakugawa ◽  
Anthony J. Blazevich ◽  
...  
Keyword(s):  
Motor Unit ◽  
Repeated Measures ◽  
Discharge Rate ◽  
Motor Units ◽  
Plantar Flexors ◽  
Force Output ◽  
Persistent Inward Currents ◽  
Gastrocnemius Medialis ◽  
Inward Currents ◽  
Maximal Discharge

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.

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