Effect of training on voluntary activation of human fusimotor neurons

The study was designed to determine if human subjects could develop a strategy that would allow them to activate muscle spindle afferents selectively, without contraction or stretch of the receptor-bearing muscle. Recordings were made from 19 identified muscle spindle afferents using insulated tungsten microelectrodes inserted into motor fascicles innervating ankle dorsiflexors, ankle plantar-flexors, and intrinsic muscles of the hand. The discharge of nine of the spindle endings accelerated in voluntary contractions at low levels of effort (less than 10% of maximum force). The remaining 10 endings had relatively high thresholds for activation in voluntary contractions. Despite periods of relative freedom to move and prolonged feedback of the spindle discharge and relevant electromyographic signals, subjects did not develop a strategy with which they could activate any of the afferents selectively. The findings suggest that fusimotor neurons in awake human subjects cannot be activated voluntarily without also activating low-threshold alpha-motoneurons. This is in contrast to reports of selective activity in muscle spindle afferents in freely moving cats. There are two possible explanations: 1) the motor tasks studied in man and cat are not equivalent, or 2) there is a species difference in the control and excitability of fusimotor neurons.

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Firing properties of muscle spindles supplying the intrinsic foot muscles of humans in unloaded and freestanding conditions

Journal of Neurophysiology ◽

10.1152/jn.00539.2018 ◽

2019 ◽

Vol 121 (1) ◽

pp. 74-84 ◽

Cited By ~ 6

Author(s):

T. P. Knellwolf ◽

A. R. Burton ◽

E. Hammam ◽

V. G. Macefield

Keyword(s):

Muscle Spindle ◽

Postural Sway ◽

Center Of Pressure ◽

Muscle Spindles ◽

Medial Malleolus ◽

Proprioceptive Information ◽

Muscle Spindle Afferents ◽

Tungsten Microelectrode ◽

Firing Properties ◽

Intrinsic Muscles

We recently developed an approach for recording from muscle spindles in the intrinsic muscles of the foot in freestanding humans by inserting a tungsten microelectrode into the posterior tibial nerve behind the medial malleolus of the ankle. Here we characterize the behavior of muscle spindles in the small muscles of the foot in 1) seated subjects with the leg horizontal and the foot naturally plantarflexed and 2) standing subjects. In the first study, recordings were made from 26 muscle spindle afferents located within flexor digiti minimi brevis ( n = 4), abductor digiti minimi ( n = 3), quadratus plantae ( n = 3), plantar interossei ( n = 4), flexor digitorum brevis ( n = 3), dorsal interossei ( n = 2), and lumbricals ( n = 2), with one each supplying abductor hallucis, adductor hallucis, and flexor hallucis brevis. The identity of another two muscle afferents was unknown. The majority of the units were silent at rest, only seven (27%) being spontaneously active. Because of the anatomic constraints of the foot, some spindles supplying muscles acting on the toes responded to movements of one or more digits. In the second study, 12 muscle spindle afferents were examined during standing. The ongoing discharge of eight spindle afferents covaried with changes in the center of pressure during postural sway. We conclude that the majority of spindle endings in the small muscles of the foot are silent at rest, which may allow them to encode changes in conformation of the foot when it is loaded during standing. Moreover, these muscle spindle afferents can provide useful proprioceptive information during standing and postural sway. NEW & NOTEWORTHY We have characterized the firing properties of muscle spindles in the intrinsic muscles of the human foot for the first time. The majority of the spindle endings are silent in seated subjects, and most fire tonically during standing, their discharge covarying with center of pressure during postural sway. We conclude that spindle endings in the intrinsic muscles of the foot provide useful proprioceptive information during free standing.

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Effects of tonic muscle pain on fusimotor control of human muscle spindles during isometric ankle dorsiflexion

Journal of Neurophysiology ◽

10.1152/jn.00862.2018 ◽

2019 ◽

Vol 121 (4) ◽

pp. 1143-1149

Author(s):

Lyndon J. Smith ◽

Vaughan G. Macefield ◽

Ingvars Birznieks ◽

Alexander R. Burton

Keyword(s):

Muscle Spindle ◽

Muscle Pain ◽

Tibialis Anterior Muscle ◽

Muscle Spindles ◽

Muscle Spindle Afferents ◽

Firing Rates ◽

Leg Muscles ◽

Tonic Muscle ◽

Voluntary Contractions ◽

Ankle Dorsiflexors

Studies on anesthetized animals have revealed that nociceptors can excite fusimotor neurons and thereby change the sensitivity of muscle spindles to stretch; such nociceptive reflexes have been suggested to underlie the mechanisms that lead to chronic musculoskeletal pain syndromes. However, the validity of the “vicious cycle” hypothesis in humans has yielded results contrasting with those found in animals. Given that spindle firing rates are much lower in humans than in animals, it is possible that some of the discrepancies between human experimental data and those obtained in animals could be explained by differences in background fusimotor drive when the leg muscles are relaxed. We examined the effects of tonic muscle pain during voluntary contractions of the ankle dorsiflexors. Unitary recordings were obtained from 10 fusimotor-driven muscle spindle afferents (6 primary, 4 secondary) supplying the ankle dorsiflexors via a microelectrode inserted percutaneously into the common peroneal nerve. A series of 1-min weak contractions was performed at rest and during 1 h of muscle pain induced by intramuscular infusion of 5% hypertonic saline into the tibialis anterior muscle. We did not observe any statistically significant increases in muscle spindle firing rates of six afferents followed during tonic muscle pain, although discharge variability increased slightly. Furthermore, a participant’s capacity to maintain a constant level of force, while relying on proprioceptive feedback in the absence of visual feedback, was not compromised during pain. We conclude that nociceptive inputs from contracting muscle do not excite fusimotor neurons during voluntary isometric contractions in humans. NEW & NOTEWORTHY Data obtained in the cat have shown that muscle pain causes a marked increase in the firing of muscle spindles, attributed to a nociceptor-driven fusimotor reflex. However, our studies of muscle spindles in relaxed leg muscles failed to find any effect on spindle discharge. Here we showed that experimental muscle pain failed to increase the firing of muscle spindle afferents during weak voluntary contractions, when fusimotor drive sufficient to increase their firing is present.

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Voluntary activation of human quadriceps during and after isokinetic exercise

Journal of Applied Physiology ◽

10.1152/jappl.1991.71.6.2122 ◽

1991 ◽

Vol 71 (6) ◽

pp. 2122-2126 ◽

Cited By ~ 46

Author(s):

D. J. Newham ◽

T. McCarthy ◽

J. Turner

Keyword(s):

Human Subjects ◽

Knee Extension ◽

Voluntary Activation ◽

Isometric Contractions ◽

Knee Angle ◽

Lower Velocity ◽

Isokinetic Contractions ◽

Normal Human ◽

Voluntary Contractions ◽

The Relationship

The extent of voluntary activation in fresh and fatigued quadriceps muscles was investigated during isometric and isokinetic voluntary contractions at 20 and 150 degrees/s in 23 normal human subjects. The muscles were fatigued by a total of 4 min of maximal knee extension at an angular velocity of 85 degrees/s. Voluntary activation was determined by the superimposition of tetanic electrical stimulation at 100 Hz for 250 ms, initiated at a constant knee angle. The relationship between voluntary and stimulated force was similar to that found with the established twitch superimposition technique used on isometric contractions. In fresh muscle all the subjects showed full voluntary activation during isometric contractions. Some activation failure was seen in five subjects at 20 degrees/s [2.0 +/- 0.9 degrees (SE)] and in two subjects at 150 degrees/s (0.7 +/- 0.5). After fatigue all subjects showed some activation failure at 0 and 20 degrees/s (36.4 +/- 3.1 and 28.8 +/- 4.1 degrees, respectively), but only two showed any at 150 degrees/s (1.4 +/- 5.7). We conclude that brief high-intensity dynamic exercise can cause a considerable failure of voluntary activation. This failure was most marked during isometric and the lower-velocity isokinetic contractions. Thus a failure of voluntary activation may have greater functional significance than previous studies of isometric contractions have indicated.

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Component of muscle spindle discharge related to arterial pulse

Journal of Neurophysiology ◽

10.1152/jn.1981.46.4.788 ◽

1981 ◽

Vol 46 (4) ◽

pp. 788-796 ◽

Cited By ~ 13

Author(s):

B. McKeon ◽

D. Burke

Keyword(s):

Blood Flow ◽

Muscle Spindle ◽

Time Course ◽

Discharge Rate ◽

Human Subjects ◽

Arterial Blood Flow ◽

Arterial Pulse ◽

Muscle Spindle Afferents ◽

Arterial Blood ◽

Doppler Flowmeter

1. In human subjects microelectrode recordings were made from 25 muscle spindle afferents from the pretibial muscles. 2. The spike discharges of three endings were locked in time to the arterial pulse. With 17 of the remaining endings, there was a significant pulse-related modulation of discharge rate. For these 20 endings the latency to the onset of the pulse-related influence was 200-310 ms. 3. The time course of the modulation of discharge rate was similar to that of arterial blood flow, as estimated using a Doppler flowmeter. With four endings occlusion of blood flow using a sphygmomanometer cuff reduced any modulation. 4. For five endings the contribution by the arterial modulation to the variance of discharge of the ending was 3-54%. For the population of endings there was no significant relationship between the depth of modulation and coefficient of variation. 5. It is concluded that the arterial pulse can be significant contributor to the variability of muscle spindle discharge. The pulsatile effects seen in the responses of single afferents are unlikely to be eliminated in the summed activity forming the population response. This could constitute a limitation of the information capacity of the population of muscle spindle afferents.

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Discharge Patterns in Human Muscle Spindle Afferents during Isometric Voluntary Contractions

Acta Physiologica Scandinavica ◽

10.1111/j.1748-1716.1970.tb04823.x ◽

1970 ◽

Vol 80 (4) ◽

pp. 552-566 ◽

Cited By ~ 106

Author(s):

Å. B. Vallbo

Keyword(s):

Muscle Spindle ◽

Human Muscle ◽

Muscle Spindle Afferents ◽

Discharge Patterns ◽

Voluntary Contractions

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Dynamic response of human muscle spindle afferents to stretch

Journal of Neurophysiology ◽

10.1152/jn.1990.63.6.1297 ◽

1990 ◽

Vol 63 (6) ◽

pp. 1297-1306 ◽

Cited By ~ 114

Author(s):

B. B. Edin ◽

A. B. Vallbo

Keyword(s):

Dynamic Response ◽

Muscle Spindle ◽

Human Subjects ◽

Muscle Afferents ◽

Human Muscle ◽

Golgi Tendon Organ ◽

Muscle Spindle Afferents ◽

Partial Data ◽

Extensor Muscles ◽

Tendon Organ

1. One hundred and twenty-four muscle afferents from the finger extensor muscles were recorded from the radial nerve in human subjects. 2. The afferents were provisionally classified as muscle spindle primary (78/124) and secondary afferents (25/124), and Golgi tendon organ afferents (21/124), on the basis of their response to 1) maximal twitch contractions, 2) 20- and 50-Hz sinusoids superimposed on ramp-and-hold stretches, 3) stretch sensitization, and 4) isometric contractions and sudden relaxations. 3. Ramp-and-hold stretches at two velocities, 10 and 50 degrees/s, were applied to the appropriate metacarpophalangeal (MCP) joint while the parent muscle remained relaxed. For each unit three discrete parameters were assessed: the presence or absence of 1) an initial burst at the commencement of the ramp stretch, 2) a deceleration response at the beginning of the hold phase, and 3) a prompt silencing at muscle shortening. In addition, two kinds of dynamic indexes were calculated for 79 of the muscle spindle afferents. 4. Most spindle afferents responded readily to stretch, whereas the Golgi tendon organ afferents produced very poor stretch responses. All of them lacked a static response, whereas the dynamic response, when present at all, consisted of only a few impulses. 5. The dynamic index was higher for spindle primaries than for secondaries, and this difference was statistically significant although the distribution was unimodal for spindle afferents as a group. Hence, this parameter was a poor discriminator. 6. Initial bursts, deceleration responses, and silences during imposed shortening were more common in spindle primaries than in secondaries. The differences were significant in all these respects. 7. The three discrete parameters were statistically pairwise independent for the spindle afferents, justifying the combination of the three into a useful battery for discrimination between primary and secondary spindle afferents and the use of this battery as a partial data base for a probability approach towards a solid classification of human muscle afferents.

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High-frequency oscillations in human electromyograms during voluntary contractions

Journal of Neurophysiology ◽

10.1152/jn.1986.56.2.542 ◽

1986 ◽

Vol 56 (2) ◽

pp. 542-553 ◽

Cited By ~ 66

Author(s):

E. N. Bruce ◽

L. M. Ackerson

Keyword(s):

High Frequency ◽

Human Subjects ◽

Power Spectra ◽

Respiratory Muscles ◽

Muscular Contraction ◽

Voluntary Activation ◽

High Frequency Oscillations ◽

Frequency Components ◽

Left And Right ◽

Voluntary Contractions

Spectral analysis was used to identify correlated sinusoidal frequency components in left and right side diaphragm electromyographic (EMG) recordings from human subjects during voluntary deep inspirations. In 31 of 33 subjects bilaterally correlated high-frequency oscillations were found in broad or narrow bands in the range of 60-84 and 16-40 Hz. To determine if such oscillations were associated also with bilaterally symmetric, phasic, voluntary activation of nonrespiratory muscles, we obtained EMG signals from left and right masseter muscles during clenching of the jaw; left and right sternomastoid muscles during lifting of the head against gravity; and left and right biceps muscles during lifting of a weighted bar. Weakly correlated frequency components, mainly at frequencies below 60 Hz, were found in the left and right masseter EMGs on at least one trial from 12 of 17 subjects. No bilaterally correlated frequency components were found during phasic contraction of biceps and sternomastoid muscles. Power spectra of biceps EMGs, however, sometimes exhibited peaks indicative of oscillations that were not bilaterally correlated. In nine subjects, correlated frequency components in the 60-84 Hz range were found in intercostal EMGs from the axillary region of the fifth interspace during voluntary deep inspirations but not during postural contractions. We conclude that high-frequency oscillations in the range of 60-84 Hz in diaphragm and intercostal EMGs are associated particularly with respiratory activation of respiratory muscles. These results support the hypothesis that high-frequency oscillations may be a manifestation of control of muscular contraction via a central pattern generator.

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In-parallel and in-series behavior of human muscle spindle endings

Journal of Neurophysiology ◽

10.1152/jn.1987.58.2.417 ◽

1987 ◽

Vol 58 (2) ◽

pp. 417-426 ◽

Cited By ~ 34

Author(s):

D. Burke ◽

A. M. Aniss ◽

S. C. Gandevia

Keyword(s):

Muscle Spindle ◽

Motor Behavior ◽

Human Subjects ◽

Motor Units ◽

Mechanical Coupling ◽

Relaxation Phase ◽

In Series ◽

Contraction And Relaxation ◽

Voluntary Contractions ◽

Muscle Spindle Endings

1. The responses of 62 putative muscle spindle afferents innervating the pretibial flexor muscles of normal human subjects were studied during graded twitch contractions of the receptor-bearing muscle to search for possible in-series coupling between spindle endings and motor units. 2. The majority of afferents (n = 57) responded unequivocally in an in-parallel manner to the twitch contractions, regardless of contraction strength. There were two patterns of in-parallel response: afferents without background activity discharged during the relaxation phase of the twitch; afferents with a background discharge were transiently silenced during the contraction phase and resumed their discharge on the relaxation phase. 3. Evidence of in-series coupling was found for five afferents during submaximal twitch contractions, to which each afferent responded in a mixed “biphasic” manner, with increases in discharge during both the contraction and relaxation phases of the twitch. Background discharge, response to stretch, and response during isometric voluntary contractions suggested that four of the afferents innervated primary spindle endings and the fifth a secondary spindle ending. 4. It is argued that the five atypical spindle endings responded in an ambiguous manner during twitch contractions of the receptor-bearing muscle because there was an in-series mechanical coupling between motor units and the spindle. The incidence of demonstrable in-series responses has serious implications for the mechanisms of spindle activation during normal motor behavior, but has only minor implications for the use of the twitch test to identify muscle spindle endings.

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Quadriceps activation during maximal isometric and isokinetic contractions: The minimal real difference and its implications

Isokinetics and Exercise Science ◽

10.3233/ies-203241 ◽

2020 ◽

pp. 1-13

Author(s):

Luigi Catino ◽

Chiara Malloggi ◽

Stefano Scarano ◽

Valeria Cerina ◽

Viviana Rota ◽

...

Keyword(s):

Intraclass Correlation ◽

Correlation Coefficients ◽

Voluntary Activation ◽

Real Difference ◽

Concentric Contractions ◽

Rehabilitation Programs ◽

Logit Transformation ◽

Isokinetic Contractions ◽

Electrical Stimuli ◽

Voluntary Contractions

BACKGROUND: A method of measurement of voluntary activation (VA, percent of full muscle recruitment) during isometric and isokinetic concentric contractions of the quadriceps femoris (QF) at 60∘/s and 120∘/s was previously validated. OBJECTIVE: This study aimed to quantify the test-retest minimal real difference (MRD) of VA during isometric (ISOM) and isokinetic concentric contractions of QF (100∘/s, ISOK) in a sample of healthy individuals. METHODS: VA was measured through the interpolated twitch technique. Pairs of electrical stimuli were delivered to the QF at 40∘ of knee flexion during maximal voluntary contractions. Twenty-five healthy participants (20–38 years, 12 women, 13 men) completed two testing sessions with a 14-day interval. VA values were linearized through logit transformation (VAl). The MRD was estimated from intraclass correlation coefficients (model 2.1). RESULTS: The VA (median, range) was 84.20% (38.2–99.9%) in ISOM and 94.22% (33.8-100%) in ISOK. MRD was 0.78 and 1.12 logit for ISOM and ISOK, respectively. As an example, in terms of percent VA these values correspond to a change from 76% to 95% and from 79% to 98% in ISOM and in ISOK, respectively. CONCLUSIONS: The provided MRD values allow to detect significant individual changes in VA, as expected after training and rehabilitation programs.

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