A comparison of peripheral and rubrospinal synaptic input to slow and fast twitch motor units of triceps surae

1. Composite group Ia excitatory postsynaptic potentials (EPSPs) produced by heteronymous nerve stimulation were recorded from triceps surae motoneurons of barbiturate-anesthetized cats. Motoneuron rheobase, input resistance, and axonal conduction velocity were measured, and motor units were classified on the basis of the mechanical responses of their muscle units. 2. The amplitude of EPSPs recorded from 33 medial gastrocnemius (MG) motoneurons ranged from 0.6 to 4.3 mV. The mean EPSP amplitude differed among the major MG motor-unit types, increasing in the order fast twitch, fast fatiguing (FF); fast twitch, fatigue resistant (FR); slow twitch, fatigue resistant (S) (FF less than FR less than S). The amplitude of EPSPs recorded from 15 soleus motoneurons ranged from 0.3 to 3.4 mV, with a mean of 1.4 mV. 3. Presynaptic inhibition of EPSPs was produced by trains of conditioning volleys in the posterior biceps-semitendinosus (PBST) nerve. In 33 MG cells PBST conditioning stimulation reduced the amplitude of EPSPs by 11-50%, with a mean inhibition of 27%. The amplitude of EPSPs in 15 soleus motoneurons was decreased by 5-84%, with a mean inhibition of 37%. 4. When the magnitude of presynaptic inhibition was expressed as percent inhibition, there was no relation between presynaptic inhibition and either motor-unit type or the amplitude of the EPSP. However, when presynaptic inhibition was expressed as the absolute amount of inhibition in millivolts, the magnitude of inhibition was highly correlated with EPSP amplitude both across the entire triceps surae population (MG, lateral gastrocnemius, soleus) as well as within each muscle population. This correlation was also significant within the MG FF and FR motor-unit populations. 5. We conclude that EPSP amplitude and not motor-unit type is the major determinant of the magnitude of presynaptic inhibition. However, because of the effect of motor-unit type on EPSP amplitude, the net effect is that presynaptic inhibition increases in the order FF less than FR less than S.

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Less common synaptic input between muscles from the same group allows for more flexible coordination strategies during a fatiguing task

Journal of Neurophysiology ◽

10.1152/jn.00453.2021 ◽

2022 ◽

Author(s):

Julien Rossato ◽

Kylie J. Tucker ◽

Simon Avrillon ◽

Lilian Lacourpaille ◽

Ales Holobar ◽

...

Keyword(s):

Synaptic Input ◽

Vastus Lateralis ◽

Rectus Femoris ◽

Motor Units ◽

The Other ◽

Triceps Surae ◽

Strong Positive Correlation ◽

Neural Drive ◽

Coordination Strategies ◽

Common Drive

This study aimed to determine whether neural drive is redistributed between muscles during a fatiguing isometric contraction, and if so, whether the initial level of common synaptic input between these muscles constrains this redistribution. We studied two muscle groups: triceps surae (14 participants) and quadriceps (15 participants). Participants performed a series of submaximal isometric contractions and a torque-matched contraction maintained until task failure. We used high-density surface electromyography to identify the behavior of 1874 motor units from the soleus, gastrocnemius medialis (GM), gastrocnemius lateralis(GL), rectus femoris, vastus lateralis (VL), and vastus medialis(VM). We assessed the level of common drive between muscles in absence of fatigue using a coherence analysis. We also assessed the redistribution of neural drive between muscles during the fatiguing contraction through the correlation between their cumulative spike trains (index of neural drive). The level of common drive between VL and VM was significantly higher than that observed for the other muscle pairs, including GL-GM. The level of common drive increased during the fatiguing contraction, but the differences between muscle pairs persisted. We also observed a strong positive correlation of neural drive between VL and VM during the fatiguing contraction (r=0.82). This was not observed for the other muscle pairs, including GL-GM, which exhibited differential changes in neural drive. These results suggest that less common synaptic input between muscles allows for more flexible coordination strategies during a fatiguing task, i.e., differential changes in neural drive across muscles. The role of this flexibility on performance remains to be elucidated.

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Comparison of physiological and histochemical properties of motor units after cross-reinnervation of antagonistic muscles in the cat hindlimb

Journal of Neurophysiology ◽

10.1152/jn.1988.60.1.365 ◽

1988 ◽

Vol 60 (1) ◽

pp. 365-378 ◽

Cited By ~ 22

Author(s):

T. Gordon ◽

C. K. Thomas ◽

R. B. Stein ◽

S. Erdebil

Keyword(s):

Muscle Fibers ◽

Motor Units ◽

Triceps Surae ◽

Medial Gastrocnemius ◽

Single Motor Units ◽

Extensor Muscles ◽

Flexor Muscles ◽

The Cross ◽

Triceps Surae Muscles ◽

Fast Twitch

1. Physiological and histochemical properties of the cat ankle extensor muscles, the lateral and medial gastrocnemius, and the soleus were studied after cross-reinnervation by flexor motoneurons. 2. Tibial and common peroneal nerves were cut and cross-united in the popliteal fossa of 2- to 6-mo-old cats. Eighteen to 24 mo later, single motor units were isolated by dissection and stimulation of ventral root filaments and classified into four types: fast-twitch, fatigable (FF), fast-twitch with intermediate fatigue resistance (FI), fast-twitch, fatigue-resistant (FR), and slow, fatigue-resistant (S). Muscle fibers were classified as fast glycolytic (FG), fast, oxidative glycolytic (FOG), and slow oxidative (SO) on the basis of histochemical staining. 3. Although motor-unit force was normally well correlated with the size of the innervating motor axon in the cross-reinnervated muscles, the force of different unit types overlapped considerably. The reinnervated motor units also showed a higher than normal degree of fatigability. 4. The range of muscle unit forces in cross-reinnervated triceps surae muscles was the same as in the normally innervated triceps surae muscles. This range is 2-3 times greater than the flexor muscles, which the common peroneal nerve normally supplies. The range of contraction speed of units in the cross-reinnervated extensor muscles was comparable to that in the flexor muscles, consistent with a motoneuron-specific determination of muscle speed (28). 5. SO and FOG muscle fibers were found in all reinnervated triceps surae muscles, but FG fibers were only found in reinnervated medial gastrocnemius (MG) and lateral gastrocnemius (LG) muscles, consistent with previous findings of the resistance of soleus muscles to complete conversion (10, 16, 20, 21). Type grouping of muscle fibers was characteristic of the reinnervated muscles. 6. Reinnervated SO muscle fibers were larger than the corresponding fibers in normally innervated muscles as were the estimated number of muscle fibers innervated by slow motor axons. Nonetheless, the force generated by the S motor units remained relatively smaller than FR and FF units. The relative contributions of the number, cross-sectional area and specific tension to the force generation of reinnervated motor units are discussed.

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Ensemble discharge from Golgi tendon organs of cat peroneus tertius muscle

Journal of Neurophysiology ◽

10.1152/jn.1990.64.3.813 ◽

1990 ◽

Vol 64 (3) ◽

pp. 813-821 ◽

Cited By ~ 22

Author(s):

G. Horcholle-Bossavit ◽

L. Jami ◽

J. Petit ◽

R. Vejsada ◽

D. Zytnicki

Keyword(s):

Motor Unit ◽

Motor Units ◽

Good Correspondence ◽

Golgi Tendon Organs ◽

Afferent Fibers ◽

Slow Type ◽

Tendon Organs ◽

Fast Twitch ◽

Force Profiles ◽

Tendon Organ

1. The responses of individual tendon organs of the cat peroneus tertius muscle to motor-unit contractions were recorded in anesthetized cats during experiments in which all the Ib-afferent fibers from the muscle had been prepared for recording in dorsal root filaments. This was possible because the cat peroneus tertius only contains a relatively small complement of approximately 10 tendon organs. 2. Motor units of different physiological types were tested for their effects on the whole population of tendon organs in the muscle. Effects of unfused tetanic contractions were tested under both isometric and anisometric conditions. Each motor unit activated at least one tendon organ, and each tendon organ was activated by at least one motor unit. Individual slow-type units were found to act on a single or two receptors, whereas a fast-type unit could activate up to six tendon organs. 3. In one experiment, the effects of 8 motor units on 10 tendon organs were examined. One fast-twitch, fatigue resistant (FR)-type unit acted on six tendon organs, of which four were also activated by another FR unit. The contraction of each unit, on its own, elicited a range of individual responses, from weak to strong. The discharge frequencies of individual responses displayed no clear relation with the strength of contraction, nor did they accurately represent the shape of force profiles. But when all the discharges were pooled, a fairly good correspondence appeared between variations of contractile force and variations of averaged discharge frequencies.(ABSTRACT TRUNCATED AT 250 WORDS)

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Changes in diaphragm motor unit EMG during fatigue

Journal of Applied Physiology ◽

10.1152/jappl.1990.68.5.1917 ◽

1990 ◽

Vol 68 (5) ◽

pp. 1917-1926 ◽

Cited By ~ 34

Author(s):

G. C. Sieck ◽

M. Fournier

Keyword(s):

Motor Unit ◽

Fatigue Test ◽

Motor Units ◽

Evoked Force ◽

Slow Twitch ◽

The Right ◽

Fast Twitch ◽

Multiple Units ◽

Motor Unit Emg ◽

Stimulation Of

Fatigue-related changes in the waveform and root-mean-square (rms) values of evoked motor unit electromyographic (EMG) responses were studied in the right sternocostal region of the cat diaphragm. Motor units were isolated by microdissection and stimulation of C5 ventral root filaments and then classified as fast-twitch fatigable (FF), fast-twitch fatigue intermediate (FInt), fast-twitch fatigue resistant (FR), or slow-twitch (S) based on standard physiological criteria. The evoked EMG responses of S and FR units showed very little change during the fatigue test. The evoked EMG waveform and rms values of FF and FInt units displayed variable changes during the fatigue test. When changes were observed, they typically included a prolongation of the EMG waveform, a decrease in peak amplitude, and a decrease in rms value. The changes in EMG amplitude and rms values were not correlated. In more fatigable units, the decrease in force during the fatigue test generally exceeded the decrease in EMG rms values. Changes in the evoked force and EMG responses of multiple units innervated by C5 or C6 ventral roots were also examined during the fatigue test. The decrease in diaphragm force during the fatigue test closely matched the force decline predicted by the proportionate contribution of different motor unit types. However, the observed reduction in diaphragm EMG rms values during the fatigue test exceeded that predicted based on the aggregate contribution of different motor unit types. It was concluded that changes in EMG do not reflect the extent of diaphragm fatigue.

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

Journal of Neurophysiology ◽

10.1152/jn.01117.2015 ◽

2016 ◽

Vol 116 (2) ◽

pp. 611-618 ◽

Cited By ~ 7

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.

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Diaphragm neuromuscular transmission failure in aged rats

Journal of Neurophysiology ◽

10.1152/jn.00061.2019 ◽

2019 ◽

Vol 122 (1) ◽

pp. 93-104 ◽

Cited By ~ 12

Author(s):

Matthew J. Fogarty ◽

Maria A. Gonzalez Porras ◽

Carlos B. Mantilla ◽

Gary C. Sieck

Keyword(s):

Nerve Stimulation ◽

Phrenic Nerve ◽

Neuromuscular Transmission ◽

Motor Units ◽

Diaphragm Muscle ◽

Muscle Stimulation ◽

Transmission Failure ◽

Old Rats ◽

Motor Neuron Loss ◽

Fast Twitch

In aging Fischer 344 rats, phrenic motor neuron loss, neuromuscular junction abnormalities, and diaphragm muscle (DIAm) sarcopenia are present by 24 mo of age, with larger fast-twitch fatigue-intermediate (type FInt) and fast-twitch fatigable (type FF) motor units particularly vulnerable. We hypothesize that in old rats, DIAm neuromuscular transmission deficits are specific to type FInt and/or FF units. In phrenic nerve/DIAm preparations from rats at 6 and 24 mo of age, the phrenic nerve was supramaximally stimulated at 10, 40, or 75 Hz. Every 15 s, the DIAm was directly stimulated, and the difference in forces evoked by nerve and muscle stimulation was used to estimate neuromuscular transmission failure. Neuromuscular transmission failure in the DIAm was observed at each stimulation frequency. In the initial stimulus trains, the forces evoked by phrenic nerve stimulation at 40 and 75 Hz were significantly less than those evoked by direct muscle stimulation, and this difference was markedly greater in 24-mo-old rats. During repetitive nerve stimulation, neuromuscular transmission failure at 40 and 75 Hz worsened to a greater extent in 24-mo-old rats compared with younger animals. Because type IIx and/or IIb DIAm fibers (type FInt and/or FF motor units) display greater susceptibility to neuromuscular transmission failure at higher frequencies of stimulation, these data suggest that the age-related loss of larger phrenic motor neurons impacts nerve conduction to muscle at higher frequencies and may contribute to DIAm sarcopenia in old rats. NEW & NOTEWORTHY Diaphragm muscle (DIAm) sarcopenia, phrenic motor neuron loss, and perturbations of neuromuscular junctions (NMJs) are well described in aged rodents and selectively affect FInt and FF motor units. Less attention has been paid to the motor unit-specific aspects of nerve-muscle conduction. In old rats, increased neuromuscular transmission failure occurred at stimulation frequencies where FInt and FF motor units exhibit conduction failures, along with decreased apposition of pre- and postsynaptic domains of DIAm NMJs of these units.

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Common Synaptic Input to the Human Hypoglossal Motor Nucleus

Journal of Neurophysiology ◽

10.1152/jn.00766.2010 ◽

2011 ◽

Vol 105 (1) ◽

pp. 380-387 ◽

Cited By ~ 20

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.

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Properties of self-reinnervated motor units of medial gastrocnemius of cat. II. Axotomized motoneurons and time course of recovery

Journal of Neurophysiology ◽

10.1152/jn.1986.55.5.947 ◽

1986 ◽

Vol 55 (5) ◽

pp. 947-965 ◽

Cited By ~ 71

Author(s):

R. C. Foehring ◽

G. W. Sypert ◽

J. B. Munson

Keyword(s):

Electrical Properties ◽

Motor Unit ◽

Fatigue Resistance ◽

Time Course ◽

Muscle Fibers ◽

Motor Units ◽

Input Resistance ◽

Medial Gastrocnemius ◽

Muscle Properties ◽

Fast Twitch

This study tested the hypothesis that functional connection to muscle is necessary for expression of normal motoneuron electrical properties. Also examined was the time course of self-reinnervation. Properties of individual medial gastrocnemius (MG) motor units were examined following section and reanastomosis of the MG nerve. Stages examined were 3-5 wk (prior to reinnervation, no-re), 5-6 wk (low-re), 9-10 wk (med-re), and 9 mo (long-re, preceding paper) after nerve section. Motor units were classified on the basis of their mechanical response as type fast twitch, fast fatiguing (FF), fast twitch with intermediate fatigue resistance (FI), fast twitch, fatigue resistant (FR), or slow twitch, fatigue resistant (S) (11, 24). Motoneuron electrical properties were measured. Muscle fibers were classified using histochemical methods as type fast glycolytic (FG), fast oxidative glycolytic (FOG), or slow oxidative (SO) (60). Prior to functional reinnervation, MG motoneurons exhibited increased input resistance, decreased rheobase, decreased rheobase/input resistance, and decreased axonal conduction velocity. There was no change in mean afterhyperpolarization (AHP) half-decay time. Normal relationships between motoneuron electrical properties were lost. These data are consistent with dedifferentiation of motoneuron properties following axotomy (35, 47). At 5-6 wk after reanastomosis, motor-unit tensions were small, and motoneuron membrane electrical properties were unchanged from the no-re stage. There were no differences in motoneuron electrical properties between cells that elicited muscle contraction and those that did not. Motor-unit types were first recognizable at the med-re stage. The proportions of fast and slow motor units were similar to normal MG. Within the fast units, there were fewer type-FF units and more type-FI and type-FR units than normal, reflecting a general increase in fatigue resistance at this stage. Neither motoneuron membrane electrical properties nor muscle contractile properties had reached normal values, although both were changed in that direction from the low-re stage. Normal relationships between muscle properties, between motoneuron properties, and between motoneuron and muscle properties were re-established. The correspondence between motor-unit type and motoneuron type was similar to normal or 9 mo reinnervated MG. Muscle-unit tetanic tensions became larger with time after reinnervation. Most of the increase in muscle tension beyond the med-re stage could be accounted for by increase in muscle fiber area. There was an increased proportion of SO muscle fibers observed in the med-re muscles, as at the long-re stage.(ABSTRACT TRUNCATED AT 400 WORDS)

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