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

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.

2009 ◽  
Vol 102 (4) ◽  
pp. 2026-2038 ◽  
Author(s):  
Carol J. Mottram ◽  
Nina L. Suresh ◽  
C. J. Heckman ◽  
Monica A. Gorassini ◽  
William Z. Rymer

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.


2013 ◽  
Vol 110 (12) ◽  
pp. 2863-2872 ◽  
Author(s):  
Jessica M. D'Amico ◽  
Ş. Utku Yavuz ◽  
Ahmet Saraçoğlu ◽  
Elif Sibel Atiş ◽  
Monica A. Gorassini ◽  
...  

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.


2001 ◽  
Vol 86 (4) ◽  
pp. 1972-1982 ◽  
Author(s):  
David J. Bennett ◽  
Yunru Li ◽  
Philip J. Harvey ◽  
Monica Gorassini

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.


2016 ◽  
Vol 116 (2) ◽  
pp. 611-618 ◽  
Author(s):  
Jakob L. Dideriksen ◽  
Ales Holobar ◽  
Deborah Falla

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.


2011 ◽  
Vol 105 (1) ◽  
pp. 380-387 ◽  
Author(s):  
Christopher M. Laine ◽  
E. Fiona Bailey

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.


1993 ◽  
Vol 70 (4) ◽  
pp. 1433-1439 ◽  
Author(s):  
B. D. Clark ◽  
S. M. Dacko ◽  
T. C. Cope

1. An attempt was made to repeat the observation that cutaneous input to the cat medial gastrocnemius (MG) muscle sometimes had the differential effect of inhibiting motoneurons with slow axonal conduction velocity while simultaneously exciting others with fast conduction velocity. Dual microelectrode recording from intact ventral root filaments was used to study the effects of cutaneous inputs on recruitment order and on firing frequency of physiologically characterized MG motor units in decerebrate cats. Motor responses to pinch of the skin over the lateral surface of the ankle as well as electrical stimulation of the caudal cutaneous sural (CCS) nerve were contrasted with the responses to static muscle stretch as well as muscle vibration. 2. In contrast to the prediction, recruitment order in pairwise tests was the same for skin pinch or CCS stimulation as it was for MG stretch or vibration in all 32 tested pairs of motor units. This sample included seven pairs comprising one slow-twitch (S) and one fast-twitch motor unit, where the predicted reversal of recruitment should have been most apparent. Regardless of the source of excitation, recruitment of motor units of the MG was consistent with Henneman's size principle in approximately 90% of trials. 3. Skin pinch increased the firing rate of 30 of 32 individual motor units previously activated by stretch or vibration, including 7 slow-twitch units. In the remaining two units, skin pinch transiently (100-400 ms) slowed the firing of an S unit in 11 of 13 vibration + pinch trials. The other unit (type unknown) showed one or two retarded spikes in each of four vibration + pinch trials. In three S units, including the lone inhibitable unit and two others that were only excited by skin pinch, there was a significant positive rank correlation between change in unit firing frequency and change in soleus integrated electromyographic activity.(ABSTRACT TRUNCATED AT 400 WORDS)


1998 ◽  
Vol 23 (1) ◽  
pp. 87-94 ◽  
Author(s):  
Christopher Rich ◽  
George L. O′Brien ◽  
Enzo Cafarelli

Motor unit firing rates in human muscle can be determined from recordings made with small-diameter microelectrodes inserted directly into the muscle during voluntary contraction. Frequently, these counts are pooled to give an average motor unit firing rate under a given set of conditions. Since the fibers of one motor unit are dispersed among the cells of several others, it is conceivable that discharge rates can be measured in more than one cell from the same unit. If this occurred frequently, the distribution of firing rates could be influenced by those from units counted more than once. Based on literature values, we made the following assumptions: vastus lateralis contains approximately 300 motor units, with an average innervation ratio of 1500. Muscle cell diameter is about 50 to 100 μm and cells are randomly distributed over a motor unit territory of 10 μm diameter. The recording range of a microelectrode is about 600 μm. Given the distribution of cells normally found in whole human muscle, the probability of recording from two or more cells of the same motor unit at 50% MVC follows a Poisson distribution with a mean of 0.44. This model suggests that although there is a low probability of some duplication in this technique, the extent to which it influences the distribution of average motor unit firing rates is minimal over the entire range of forces produced by vastus lateralis. Key words: probability, motor unit, single unit recording, human muscle, rate coding


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.


2008 ◽  
Vol 33 (6) ◽  
pp. 1086-1095 ◽  
Author(s):  
Teatske M. Altenburg ◽  
Cornelis J. de Ruiter ◽  
Peter W.L. Verdijk ◽  
Willem van Mechelen ◽  
Arnold de Haan

A single shortening contraction reduces the force capacity of muscle fibers, whereas force capacity is enhanced following lengthening. However, how motor unit recruitment and discharge rate (muscle activation) are adapted to such changes in force capacity during submaximal contractions remains unknown. Additionally, there is limited evidence for force enhancement in larger muscles. We therefore investigated lengthening- and shortening-induced changes in activation of the knee extensors. We hypothesized that when the same submaximal torque had to be generated following shortening, muscle activation had to be increased, whereas a lower activation would suffice to produce the same torque following lengthening. Muscle activation following shortening and lengthening (20° at 10°/s) was determined using rectified surface electromyography (rsEMG) in a 1st session (at 10% and 50% maximal voluntary contraction (MVC)) and additionally with EMG of 42 vastus lateralis motor units recorded in a 2nd session (at 4%–47%MVC). rsEMG and motor unit discharge rates following shortening and lengthening were normalized to isometric reference contractions. As expected, normalized rsEMG (1.15 ± 0.19) and discharge rate (1.11 ± 0.09) were higher following shortening (p < 0.05). Following lengthening, normalized rsEMG (0.91 ± 0.10) was, as expected, lower than 1.0 (p < 0.05), but normalized discharge rate (0.99 ± 0.08) was not (p > 0.05). Thus, muscle activation was increased to compensate for a reduced force capacity following shortening by increasing the discharge rate of the active motor units (rate coding). In contrast, following lengthening, rsEMG decreased while the discharge rates of active motor units remained similar, suggesting that derecruitment of units might have occurred.


Author(s):  
Carina Marconi Germer ◽  
Dario Farina ◽  
Leonardo Abdala Elias ◽  
Stefano Nuccio ◽  
François Hug ◽  
...  

Crosstalk is an important source of error in interpreting surface electromyography (EMG) signals. Here, we aimed at characterizing crosstalk for three groups of synergistic muscles by the identification of individual motor unit action potentials. Moreover, we explored whether spatial filtering (single and double differential) of the EMG signals influences the level of crosstalk. Three experiments were conducted. Participants (total twenty-five) performed isometric contractions at 10% of the maximal voluntary contraction (MVC) with digit muscles and knee extensors, and at 30% MVC with plantar flexors. High-density surface EMG signals were recorded and decomposed into motor unit spike trains. For each muscle, we quantified the crosstalk induced to neighboring muscles and the level of contamination by the nearby muscle activity. We also estimated the influence of crosstalk on the EMG power spectrum and intermuscular correlation. Most motor units (80%) generated significant crosstalk signals to neighboring muscle EMG in monopolar recording mode, but this proportion decreased with spatial filtering (50% and 42% for single and double differential, respectively). Crosstalk induced overestimations of intermuscular correlation and has a small effect on the EMG power spectrum, which indicates that crosstalk is not reduced with high-pass temporal filtering. Conversely, spatial filtering diminished the crosstalk magnitude and the overestimations of intermuscular correlation, confirming to be an effective and simple technique to reduce crosstalk. This paper presents a new method for the identification and quantification of crosstalk at the motor unit level and clarifies the influence of crosstalk on EMG interpretation for muscles with different anatomy.


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