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

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.

scholarly journals Muscle spindles in human tibialis anterior encode muscle fascicle length changes

2017 ◽  
Vol 117 (4) ◽  
pp. 1489-1498 ◽  
Author(s):  
James Day ◽  
Leah R. Bent ◽  
Ingvars Birznieks ◽  
Vaughan G. Macefield ◽  
Andrew G. Cresswell
Keyword(s):  
Muscle Spindle ◽  
Tibialis Anterior ◽  
Tibialis Anterior Muscle ◽  
Muscle Length ◽  
Muscle Spindles ◽  
Muscle Spindle Afferents ◽  
Fascicle Length ◽  
Muscle Fascicle ◽  
Length Changes

Muscle spindles provide exquisitely sensitive proprioceptive information regarding joint position and movement. Through passively driven length changes in the muscle-tendon unit (MTU), muscle spindles detect joint rotations because of their in-parallel mechanical linkage to muscle fascicles. In human microneurography studies, muscle fascicles are assumed to follow the MTU and, as such, fascicle length is not measured in such studies. However, under certain mechanical conditions, compliant structures can act to decouple the fascicles, and, therefore, the spindles, from the MTU. Such decoupling may reduce the fidelity by which muscle spindles encode joint position and movement. The aim of the present study was to measure, for the first time, both the changes in firing of single muscle spindle afferents and changes in muscle fascicle length in vivo from the tibialis anterior muscle (TA) during passive rotations about the ankle. Unitary recordings were made from 15 muscle spindle afferents supplying TA via a microelectrode inserted into the common peroneal nerve. Ultrasonography was used to measure the length of an individual fascicle of TA. We saw a strong correlation between fascicle length and firing rate during passive ankle rotations of varying rates (0.1–0.5 Hz) and amplitudes (1–9°). In particular, we saw responses observed at relatively small changes in muscle length that highlight the sensitivity of the TA muscle to small length changes. This study is the first to measure spindle firing and fascicle dynamics in vivo and provides an experimental basis for further understanding the link between fascicle length, MTU length, and spindle firing patterns. NEW & NOTEWORTHY Muscle spindles are exquisitely sensitive to changes in muscle length, but recordings from human muscle spindle afferents are usually correlated with joint angle rather than muscle fascicle length. In this study, we monitored both muscle fascicle length and spindle firing from the human tibialis anterior muscle in vivo. Our findings are the first to measure these signals in vivo and provide an experimental basis for exploring this link further.

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

2019 ◽  
Vol 121 (1) ◽  
pp. 74-84 ◽  
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.

scholarly journals The effects of vibration-induced altered stretch reflex sensitivity on maximal motor unit firing properties

2019 ◽  
Vol 121 (6) ◽  
pp. 2215-2221 ◽  
Author(s):  
Alejandra Barrera-Curiel ◽  
Ryan J. Colquhoun ◽  
Jesus A. Hernandez-Sarabia ◽  
Jason M. DeFreitas
Keyword(s):  
Motor Unit ◽  
Muscle Spindle ◽  
Stretch Reflex ◽  
Muscle Spindles ◽  
Motor Unit Action Potential ◽  
Firing Rates ◽  
Motor Unit Firing ◽  
Firing Properties ◽  
Spindle Function ◽  
Voluntary Strength

It is well known that muscle spindles have a monosynaptic, excitatory connection with α-motoneurons. However, the influence of muscle spindles on human motor unit behavior during maximal efforts remains untested. It has also been shown that muscle spindle function, as assessed by peripheral reflexes, can be systematically manipulated with muscle vibration. Therefore, the purpose of this study was to analyze the effects of brief and prolonged vibration on maximal motor unit firing properties. A crossover design was used, in which each of the 24 participants performed one to three maximal knee extensions under three separate conditions: 1) control, 2) brief vibration that was applied during the contraction, and 3) after prolonged vibration that was applied for ~20 min before the contraction. Multichannel EMG was recorded from the vastus lateralis during each contraction and was decomposed into its constituent motor unit action potential trains. Surprisingly, an approximate 9% reduction in maximal voluntary strength was observed not only after prolonged vibration but also during brief vibration. In addition, both vibration conditions had a large, significant effect on firing rates (a decrease in the rates) and a small to moderate, nonsignificant effect on recruitment thresholds (a small increase in the thresholds). Therefore, vibration had a detrimental influence on both maximal voluntary strength and motor unit firing properties, which we propose is due to altered function of the stretch reflex pathway. NEW & NOTEWORTHY We used vibration to alter muscle spindle function and examined the vibration’s influence on maximal motor unit properties. We discovered that vibration had a detrimental influence on motor unit behavior and motor output by decreasing motor unit firing rates, increasing recruitment thresholds, which led to decreased maximal strength. We believe that understanding the role of muscle spindles during maximal contractions provides a deeper insight into motor control and sensorimotor integration.

Responses of cat peroneus brevis muscle spindle afferents during recovery from nerve-crush injury

1983 ◽  
Vol 50 (2) ◽  
pp. 344-357 ◽  
Author(s):  
D. Hyde ◽  
J. J. Scott
Keyword(s):  
Muscle Spindle ◽  
Common Peroneal Nerve ◽  
Firing Frequency ◽  
Muscle Spindle Afferents ◽  
Nerve Crush ◽  
Firing Rates ◽  
The Common ◽  
Peroneus Brevis ◽  
Nerve Crush Injury ◽  
Stimulation Of

The responses of regenerated muscle spindle afferents to ramp-and-hold stretch of the peroneus brevis muscle in the cat were recorded at periods from 26 to 140 days after crushing the common peroneal nerve. During the early stages of recovery a number of abnormally responding afferents were observed. The most marked abnormality was the absence or rapid failure of firing during the held phase of the stretch. The proportion of abnormal afferents became less as recovery progressed. Electrical stimulation of isolated static and dynamic gamma-axons increased the firing rates of the afferents during the ramp-and-hold stretch such that a gamma static axon would restore the response of an abnormal afferent to the held phase of the stretch. The regenerated afferents have been classified according to the degree of abnormality displayed. These abnormalities can be accounted for by assuming a subtractive reduction in the firing frequency of the regenerated afferents. This is attributed to an increase in the pacemaker threshold.

Modulation of Jaw Muscle Spindle Discharge During Mastication in the Rabbit

1997 ◽  
Vol 77 (4) ◽  
pp. 2227-2231 ◽  
Author(s):  
Y. Masuda ◽  
T. Morimoto ◽  
O. Hidaka ◽  
T. Kato ◽  
R. Matsuo ◽  
...  
Keyword(s):  
Muscle Spindle ◽  
High Frequency ◽  
Low Frequency ◽  
Phase Relationship ◽  
Muscle Spindles ◽  
Jaw Movement ◽  
Firing Rates ◽  
Jaw Opening ◽  
Jaw Muscle ◽  
Opening Phase

Masuda, Y., T. Morimoto, O. Hidaka, T. Kato, R. Matsuo, T. Inoue, M. Kobayashi, and A. Taylor. Modulation of jaw muscle spindle discharge during mastication in the rabbit. J. Neurophysiol. 77: 2227–2231, 1997. Discharges of jaw muscle spindles were recorded during chewing carrot from mesencephalic trigeminal nucleus (Mes V) in the awake rabbit to evaluate contribution of the muscle spindles to the development of complete sequences of masticatory movements. The Mes V spindle units were divided into two types according to the maximum firing rates during mastication, with a dividing line at 200 Hz; high-frequency units and low-frequency units. Although both types of units fired maximally during the jaw-opening phase of chewing cycles, their firing rates and pattern varied according to three sequential stages of mastication (stages I, IIa, and IIb). The high-frequency units often increased firing before the start of mastication and built up firing in the first few chewing cycles. Their maximal firing rate was sometimes lower during stage IIa (chewing stage) than during stage I (ingestion stage) and stage IIb (preswallowing stage), although the jaw movements were greater in stage IIa than in other stages. The phase relationship of the firing to a jaw movement cycle in stage IIa was consistent in individual units. The low-frequency units did not build up activity before the onset of movements. They fired mostly during the jaw-opening phase, but the peak of firing did not necessarily coincide with the time of maximal opening. It was concluded that the difference in the firing pattern among masticatory stages may be ascribed to a stage-dependent modulation of both fusimotor activity and jaw movement pattern.

scholarly journals Tonic muscle pain does not increase fusimotor drive to human leg muscles: implications for chronic muscle pain

2013 ◽  
Vol 98 (6) ◽  
pp. 1125-1132 ◽  
Author(s):  
Azharuddin Fazalbhoy ◽  
Vaughan G. Macefield ◽  
Ingvars Birznieks
Keyword(s):  
Muscle Pain ◽  
Leg Muscles ◽  
Tonic Muscle ◽  
Chronic Muscle Pain

Reflex influences on muscle spindle activity in relaxed human leg muscles

1986 ◽  
Vol 56 (1) ◽  
pp. 159-170 ◽  
Author(s):  
S. C. Gandevia ◽  
S. Miller ◽  
A. M. Aniss ◽  
D. Burke
Keyword(s):  
Muscle Spindle ◽  
Tibialis Anterior ◽  
Tibial Nerve ◽  
Triceps Surae ◽  
Motor Threshold ◽  
Muscle Spindle Afferents ◽  
Posterior Tibial ◽  
Leg Muscles ◽  
Low Threshold ◽  
Electrical Stimuli

The study was designed to determine whether low-threshold cutaneous and muscle afferents from the foot reflexly activate gamma-motoneurons innervating relaxed muscles of the leg. In 15 experiments multiunit recordings were made from 21 nerve fascicles innervating triceps surae or tibialis anterior. In a further nine experiments the activity of 19 identified single muscle spindle afferents was recorded, 13 from triceps surae, 5 from tibialis anterior, and 1 from extensor digitorum longus. Trains of electrical stimuli (5 stimuli, 300 Hz) were delivered to the sural nerve at the ankle (intensity, twice sensory threshold) and the posterior tibial nerve at the ankle (intensity, 1.1 times motor threshold for the small muscles of the foot). In addition, a tap on the appropriate tendon at varying times after the stimuli was used to assess the dynamic responsiveness of the afferents under study. The conditioning electrical stimuli did not change the discharge of single spindle afferents. Recordings of rectified and averaged multiunit activity also revealed no change in the overall level of background neural activity following the electrical stimuli. The afferent responses to tendon taps did not differ significantly whether or not they were preceded by stimulation of the sural or posterior tibial nerves. These results suggest that low-threshold afferents from the foot do not produce significant activation of fusimotor neurons in relaxed leg muscles, at least as judged by their ability to alter the discharge of muscle spindle afferents. As there may be no effective background activity in fusimotor neurons innervating relaxed human muscles, it is possible that these inputs from the foot could influence the fusimotor system during voluntary contractions when the fusimotor neurons have been brought to firing threshold. In one subject trains of stimuli were delivered to the posterior tibial nerve at painful levels (30 times motor threshold). They produced an acceleration of the discharge of a spindle in soleus at a latency of approximately 125 ms, in advance of detectable activity in skeletomotor neurons and before an increase in muscle length was noted. It presumably resulted from activation of gamma-motoneurons innervating soleus by small myelinated afferents (A-delta range).

Effect of training on voluntary activation of human fusimotor neurons

1985 ◽  
Vol 54 (6) ◽  
pp. 1422-1429 ◽  
Author(s):  
S. C. Gandevia ◽  
D. Burke
Keyword(s):  
Muscle Spindle ◽  
Human Subjects ◽  
Species Difference ◽  
Voluntary Activation ◽  
Plantar Flexors ◽  
Motor Tasks ◽  
Muscle Spindle Afferents ◽  
Muscles Of The Hand ◽  
Voluntary Contractions ◽  
Intrinsic Muscles

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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