-
The Journal of Experimental Biology Aug 2019Stretches of relaxed cat and rat muscle elicit similar history-dependent muscle spindle Ia firing rates that resemble history-dependent forces seen in single activated...
Stretches of relaxed cat and rat muscle elicit similar history-dependent muscle spindle Ia firing rates that resemble history-dependent forces seen in single activated muscle fibers ( Nichols and Cope, 2004). Owing to thixotropy, whole musculotendon forces and muscle spindle firing rates are history dependent during stretch of relaxed cat muscle, where both muscle force and muscle spindle firing rates are elevated in the first stretch in a series of stretch-shorten cycles ( Blum et al., 2017). By contrast, rat musculotendon exhibits only mild thixotropy, such that the measured forces when stretched cannot explain history-dependent muscle spindle firing rates in the same way ( Haftel et al., 2004). We hypothesized that history-dependent muscle spindle firing rates elicited in stretch of relaxed rat muscle mirror history-dependent muscle fiber forces, which are masked at the level of whole musculotendon force by extracellular tissue force. We removed estimated extracellular tissue force contributions from recorded musculotendon force using an exponentially elastic tissue model. We then showed that the remaining estimated muscle fiber force resembles history-dependent muscle spindle firing rates recorded simultaneously. These forces also resemble history-dependent forces recorded in stretch of single activated fibers that are attributed to muscle cross-bridge mechanisms ( Campbell and Moss, 2000). Our results suggest that history-dependent muscle spindle firing in both rats and cats arise from history-dependent forces owing to thixotropy in muscle fibers.
Topics: Animals; Elastic Tissue; Female; Muscle Contraction; Muscle Fibers, Skeletal; Muscle Spindles; Muscle, Skeletal; Neurons, Afferent; Rats, Wistar
PubMed: 31324662
DOI: 10.1242/jeb.196287 -
The Journal of Neuroscience : the... Jun 2012Motor pools comprise a heterogeneous population of motor neurons that innervate distinct intramuscular targets. While the organization of motor neurons into motor pools...
Motor pools comprise a heterogeneous population of motor neurons that innervate distinct intramuscular targets. While the organization of motor neurons into motor pools has been well described, the time course and mechanism of motor pool diversification into functionally distinct classes remains unclear. γ-Motor neurons (γ-MNs) and α-motor neurons (α-MNs) differ in size, molecular identity, synaptic input and peripheral target. While α-MNs innervate extrafusal skeletal muscle fibers to mediate muscle contraction, γ-MNs innervate intrafusal fibers of the muscle spindle, and regulate sensitivity of the muscle spindle in response to stretch. In this study, we find that the secreted signaling molecule Wnt7a is selectively expressed in γ-MNs in the mouse spinal cord by embryonic day 17.5 and continues to molecularly distinguish γ-from α-MNs into the third postnatal week. Our data demonstrate that Wnt7a is the earliest known γ-MN marker, supporting a model of developmental divergence between α- and γ-MNs at embryonic stages. Furthermore, using Wnt7a expression as an early marker of γ-MN identity, we demonstrate a previously unknown dependence of γ-MNs on a muscle spindle-derived, GDNF-independent signal during the first postnatal week.
Topics: Animals; Biomarkers; Cell Size; Cell Survival; Female; Glial Cell Line-Derived Neurotrophic Factor; Immunohistochemistry; Mice; Mice, Knockout; Motor Neurons, Gamma; Muscle Spindles; Pregnancy; Signal Transduction; Spinal Cord; Wnt Proteins
PubMed: 22723712
DOI: 10.1523/JNEUROSCI.1160-12.2012 -
Cell Proliferation Sep 2019Muscle spindles are proprioceptive receptors in the skeletal muscle. Peripheral nerve injury results in a decreased number of muscle spindles and their morphologic...
OBJECTIVES
Muscle spindles are proprioceptive receptors in the skeletal muscle. Peripheral nerve injury results in a decreased number of muscle spindles and their morphologic deterioration. However, the muscle spindles recover when skeletal muscles are reinnervated with surgical procedures, such as nerve suture or nerve transfer. Morphological changes in muscle spindles by cell transplantation procedure have not been reported so far. Therefore, we hypothesized that transplantation of embryonic sensory neurons may improve sensory neurons in the skeletal muscle and reinnervate the muscle spindles.
MATERIALS AND METHODS
We collected sensory neurons from dorsal root ganglions of 14-day-old rat embryos and prepared a rat model of peripheral nerve injury by performing sciatic nerve transection and allowing for a period of one week before which we performed the cell transplantations. Six months later, the morphological changes of muscle spindles in the cell transplantation group were compared with the naïve control and surgical control groups.
RESULTS
Our results demonstrated that transplantation of embryonic dorsal root ganglion cells induced regeneration of sensory nerve fibre and reinnervation of muscle spindles in the skeletal muscle. Moreover, calbindin D-28k immunoreactivity in intrafusal muscle fibres was maintained for six months after denervation in the cell transplantation group, whereas it disappeared in the surgical control group.
CONCLUSIONS
Cell transplantation therapies could serve as selective targets to modulate mechanosensory function in the skeletal muscle.
Topics: Animals; Calbindins; Embryo, Mammalian; Ganglia, Spinal; Male; Muscle Spindles; Nerve Fibers; Peripheral Nerve Injuries; Rats; Rats, Inbred F344; Regeneration; Tibial Nerve
PubMed: 31264327
DOI: 10.1111/cpr.12660 -
The Journal of Physiology Oct 19711. The tension in the iliofibularis muscle of frogs was recorded while the muscle was stretched or released. At the same time recordings were made from single spindle...
1. The tension in the iliofibularis muscle of frogs was recorded while the muscle was stretched or released. At the same time recordings were made from single spindle afferents in dorsal root filaments. Either large or small motor nerve fibres were stimulated in split ventral root filaments.2. While small motor nerve fibres were stimulated the discharge from muscle spindle afferents was greatly increased by stretching, and greatly reduced by shortening the muscle. This sensitivity to movement was shown even if the movements were small, so that a stretch of 0.2% of the muscle length was sufficient to cause a pronounced increase in the afferent discharge.3. In contrast, during stimulation of the large motor nerve fibres the spindle was much less sensitive to movements with the result that even stretches or releases of the muscle by 1 mm did not cause very large changes in the discharge frequency.4. The tension in slow extrafusal muscle fibres in many ways mirrored the spindle discharge during the stimulation of small motor nerve fibres, for the tension was greatly increased by stretching, even through small distances, and greatly reduced by releasing the muscle. The tension in fast extrafusal muscle fibres was much less changed by such movements, and thus was rather like the spindle discharge during stimulation of large motor nerve fibres.5. As the extrafusal muscle fibres do not directly pull on and excite the spindle afferents, the simplest explanation for the similarities between the muscle tension and the spindle discharge is that the mechanical properties of the intrafusal muscle fibres innervated by the large motor nerve fibres are like those of fast extrafusal muscle fibres, and that the mechanical properties of the small intrafusal fibres are similar to those of slow extrafusal muscle fibres.6. It is shown that the cross-bridge sliding filament mechanism of muscle contraction provides a ready explanation for the differences found between fast and slow muscles, and it is concluded that a most important functional difference between the two sorts of intrafusal muscle fibres is the speed of their contractions, for it is this which determines their contrasting actions on the spindle.7. It was also found that low rates (< 4/sec) of small motor nerve fibre stimulation were often very effective in exciting the spindles. These rates produced rather little extrafusal tension.
Topics: Action Potentials; Animals; Anura; Electric Stimulation; Electrophysiology; In Vitro Techniques; Motor Neurons; Muscle Contraction; Muscle Spindles; Muscles; Rana pipiens; Rana temporaria
PubMed: 4257030
DOI: 10.1113/jphysiol.1971.sp009601 -
Physiological Reports Oct 2019Obesity is associated with balance and motor control deficits. We have recently shown that Group Ia muscle spindle afferents, the sensory arm of the muscle stretch...
Obesity is associated with balance and motor control deficits. We have recently shown that Group Ia muscle spindle afferents, the sensory arm of the muscle stretch reflex, are less responsive in mice fed a high-fat diet. Here we test the hypothesis that reflex excitability to sensory information from Group Ia muscle spindle afferents is altered in a mouse model of diet-induced obesity. We measured the anesthetized Hoffmann's or H-reflex, the electrical analog of the muscle stretch reflex. Adult mice of both sexes were fed a control diet (CD; 10% kcal from fat) or a high-fat diet (HFD; 60% kcal from fat) for 5, 10, or 15 weeks. We used three quantitative measures of H-reflex excitability: (1) H-reflex latency; (2) the percentage of motor neurons recruited from electrical stimulation of Group Ia muscle spindle afferents (H /M ); and (3) rate-dependent depression (RDD), the decrease in H-reflex amplitude to high frequency stimulation (20 stimuli at 5 Hz). A HFD did not significantly alter H latency (P = 0.16) or H /M ratios (P = 0.06), but RDD was significantly lower in HFD compared to CD groups (P < 0.001). Interestingly, HFD males exhibited decreased RDD compared to controls only after 5 and 10 weeks of feeding, but females showed progressive decreases in RDD that were only significant at 10 and 15 weeks on the HFD. These results suggest that high-fat feeding increases H-reflex excitability. Future studies are needed to determine whether these changes alter muscle stretch reflex strength and/or balance and to determine the underlying mechanism(s).
Topics: Animals; Diet, High-Fat; Electric Stimulation; Female; H-Reflex; Male; Mice; Motor Neurons; Muscle Contraction; Muscle Spindles; Muscle, Skeletal; Obesity; Reflex, Abnormal
PubMed: 31660698
DOI: 10.14814/phy2.14271 -
The Journal of Physiology Dec 1985The fluorescent compound Lucifer Yellow was injected into the somata of nine identified jaw-elevator muscle spindle afferents, located in the V mesencephalic nucleus....
The fluorescent compound Lucifer Yellow was injected into the somata of nine identified jaw-elevator muscle spindle afferents, located in the V mesencephalic nucleus. Reconstructions of the central course of their axons were subsequently made from serial, transverse, sections to identify sites of projection. Three sites of termination were identified on the basis of collaterals that ended in varicosities and/or boutons. All afferents projected to the V nucleus oralis and, all but one, also to the V motor nucleus. Two out of nine afferents had terminations in the supra-trigeminal nucleus, though a further four appeared to send collaterals to this area. The relative density of projection, judged by the number of collaterals supplied to each area, decreased in the order: V nucleus oralis, V motor nucleus and supra-trigeminal nucleus. The central course of the afferent axons was such that impulses from the periphery would arrive first at the V motor nucleus, then the V nucleus oralis, the supra-trigeminal nucleus, and finally the afferent somata in the V mesencephalic nucleus. In animals in which the masseter nerve was exposed in-continuity for electrical stimulation, electrophysiological recordings were made in the three areas described above to identify units that received a monosynaptic input from spindles in the masseter muscle. Criteria were formulated on the basis of the pattern of responses on stimulation of the masseter nerve, and the morphology of labelled neurones, for differentiating between afferents, interneurones, and motoneurones. In the V motor nucleus, monosynaptic excitatory post-synaptic potentials (e.p.s.p.s) were obtained in both synergist and masseter motoneurones. These were assumed to arise from a masseter muscle spindle input as the thresholds for exciting such afferents and eliciting e.p.s.p.s were similar. Some interneurones, chiefly in the V nucleus oralis, were activated at thresholds close to that of muscle spindle afferents and could also fire in response to muscle stretch. As their latencies (measured extracellularly) were similar to that of e.p.s.p.s in motoneurones, they were assumed to receive a monosynaptic muscle spindle input. However, most interneurones were activated at longer latencies (up to 7 ms) and some also fired to muscle stretch. Arguments are advanced, based on the long rise time of e.p.s.p.s recorded in some, that the majority of these may also be candidates for monosynaptic activation.(ABSTRACT TRUNCATED AT 400 WORDS)
Topics: Animals; Electrophysiology; Interneurons; Masticatory Muscles; Motor Neurons; Muscle Spindles; Neurons, Afferent; Rats; Time Factors; Trigeminal Nuclei
PubMed: 2936881
DOI: 10.1113/jphysiol.1985.sp015890 -
The Journal of Physiology Oct 19711. Impulses in single muscle afferents were recorded from the median nerves of waking human subjects with percutaneously inserted tungsten needle electrodes. During...
1. Impulses in single muscle afferents were recorded from the median nerves of waking human subjects with percutaneously inserted tungsten needle electrodes. During isometric voluntary contractions, unitary discharges were analysed from muscle spindle endings in the wrist and finger flexor muscles and the electromyographic activity from these muscles was recorded simultaneously.2. When the subject activated the muscle portion in which a spindle was located, the afferent discharge increased in spite of the mechanical unloading effects of the skeletomotor contraction indicating a concomitant fusimotor activation. This was valid for slowly rising contractions as well as small fast rising twitches.3. The time of onset of spindle acceleration was determined in relation to the time of onset of the electromyographic activity for thirty-one units studied altogether in more than seven hundred contractions. It was found that spindle acceleration regularly occurred after the onset of the electromyographic activity.4. There was a considerable variation from one test to the other, for the individual units, with regard to the exact time of onset of spindle acceleration, although spindle acceleration occurred mostly within 0.5 sec after the onset of the electromyographic activity in sustained contractions and within 0.1 sec in small fast rising twitches. It was not possible to assess to what extent this variation was accounted for by variations in the mechanical unloading effects of the skeletomotor contraction or variations in the timing of the fusimotor outflow.5. For many units, spindle acceleration did not occur until 10-50 msec after the onset of the skeletomotor contraction. This time is of the same order of magnitude as the time difference in latency from the spinal cord to the recording points in the two systems, as estimated from reasonable assumptions.6. It was concluded that the fusimotor system does not participate in the initiation of voluntary contractions in man, but that the skeletomotor activity is initiated by descending impulses from supraspinal structures and their effects on the neuronal organization within the spinal cord.7. The fact that fusimotor activation occurs also in very small and short lasting twitches, when spindle acceleration must have a negligible influence on the skeletomotor outflow, suggests that the fusimotor and the skeletomotor systems are rigidly co-activated in voluntary contractions.8. The finding that spindle acceleration does not occur until 10-50 msec after the onset of the electromyographic activity suggests that there is an approximately simultaneous onset of the fusimotor and the skeletomotor outflows from the spinal cord.
Topics: Adult; Electrodes; Electromyography; Electrophysiology; Fingers; Humans; Motor Neurons; Muscle Contraction; Muscle Spindles; Muscles; Neurons, Afferent; Spinal Cord; Time Factors; Tungsten; Wrist
PubMed: 4256547
DOI: 10.1113/jphysiol.1971.sp009625 -
The Journal of Physiology Jul 19771. Using large ramp and triangular stretches a survey has been made of the effect of stimulating single gamma fusimotor fibres on primary endings of muscle spindles in...
1. Using large ramp and triangular stretches a survey has been made of the effect of stimulating single gamma fusimotor fibres on primary endings of muscle spindles in the peroneus brevis to see whether 'intermediate' types of fusimotor action could be recognized, falling between the well known static and dynamic types. 2. Responses were classified into six groups, as detailed on pp. 844-846, ranging from apparently 'pure' dynamic action (category I) to apparently 'pure' static action (category IV). Models for a putative mixed action were produced by combining the stimulation of a static and of a dynamic fibre to the same spindle. The clearest sign of static action was firing on the releasing phase of the stretch. The essential sign of dynamic action, which survived combination with the more dominant static action, was the low adaptive decay of firing with a time constant of about 0-5 sec that occurs on the plateau of the ramp stretch. 3. Out of 153 responses, each elicited from a primary ending on stimulation of a single fusimotor fibre, 67% were apparently 'pure' examples of dynamic and static action. The remaining 33% of responses were to some degree suggestive of an admixture, in various proportions, of static and dynamic actions. For only 18% of them was there firm indication of such admixture. 4. When a given fibre was tested on more than one ending then, with one exception out of thirty-six instances, its action always proved to be either predominantly static or predominantly dynamic. There was no special tendency for an axon with a mixed action on one spindle to have a similarly mixed action on other endings so that individual fusimotor fibres were best classified as static or dynamic without intermediate grades. 5. Simultaneous stimulation of two fusimotor fibres eliciting apparently 'pure static and dynamic actions, could mimic all the intermediate types of action. 6. The results are discussed in relation to recent studies, especially those based on glycogen depletion. It was concluded that dynamic action arises from activation of the bag1 intrafusal muscle fibre, and that static action arises from the bag2 and chain fibres, whether acting individually or collaboratively. The intermediate actions are suggested to arise from an overlap of motor innervation to contrasting types of intrafusal muscle fibre. 7. On the basis of effects on the regularity of the afferent discharge the findings support the view that a given static action axon can innervate bag2 and chain fibres in various proportions in different spindles, so that they do not provide separable effector pathways. 8. Responses to large amplitude sinusoidal stretching were also studied in relation to our classification.
Topics: Action Potentials; Animals; Cats; Glycogen; Motor Neurons; Motor Neurons, Gamma; Muscle Contraction; Muscle Spindles; Neural Conduction
PubMed: 142145
DOI: 10.1113/jphysiol.1977.sp011884 -
The Journal of Physiology Jun 19881. Sixty-seven afferents from the finger extensor muscles were consecutively recorded by microneurography. 2. The units were classified as primary or secondary muscle...
1. Sixty-seven afferents from the finger extensor muscles were consecutively recorded by microneurography. 2. The units were classified as primary or secondary muscle spindle afferents or Golgi tendon organ afferents on the basis of their responses to ramp-and-hold stretches, sinusoidals superimposed on ramp-and-hold stretches, maximal twitch contractions and isometric contractions and relaxations. 3. The muscle was repeatedly stretched and then either kept short or long for a few seconds followed by a slow ramp stretch. The responses of the muscle afferents to the slow stretch were compared under the two conditions. 4. Thirty out of thirty-eight units classified as primary spindle afferents and four out of eleven units classified as secondary afferents showed an enhanced response to the slow ramp when the muscle had been kept short compared to the response when the muscle had been kept long. 5. None of the eighteen Golgi tendon organ afferents showed any difference in this respect. 6. It is concluded that stretch sensitization does occur in human muscle spindles and, when present, constitutes firm evidence of the afferent originating from a muscle spindle rather than a Golgi tendon organ. In addition, due to differences in the response characteristics of primaries and secondaries, the test may aid in separating muscle spindle primary afferents from secondary afferents.
Topics: Action Potentials; Adult; Fingers; Humans; Mechanoreceptors; Muscle Contraction; Muscle Spindles; Neurons, Afferent; Time Factors
PubMed: 2971105
DOI: 10.1113/jphysiol.1988.sp017113 -
The Journal of Physiology Aug 2002In order to investigate the nature (i.e. static or dynamic) of fusimotor drive to the flexor hallucis longus (FHL) and flexor digitorum longus (FDL) muscles during...
In order to investigate the nature (i.e. static or dynamic) of fusimotor drive to the flexor hallucis longus (FHL) and flexor digitorum longus (FDL) muscles during locomotion we recorded Ia and group II muscle spindle afferent responses to sinusoidal stretch (0.25 and 1 mm amplitude, respectively, 4-5 Hz) in a decerebrate cat preparation. FHL Ia and group II afferents generally had increased discharge rates and decreased modulation to stretch throughout the step cycle, compared to rest, suggesting raised static gamma drive at all locomotor phases. Although the modulation of Ia afferents was reduced during locomotion, most (13 of 18) showed a clear increasing trend during homonymous muscle activity (extension). This was consistent with phasic dynamic gamma drive to FHL spindles linked with alpha drive. In agreement with previous reports, FHL gave a single burst of EMG activity during the step cycle while FDL alpha drive had two components. One was related to extension while the other comprised a brief burst around the end of this phase. Typically FDL Ia and group II afferents also had elevated firing rates and reduced modulation at all locomotor phases, again implicating static gamma drive. Half the afferents (seven Ia, three group II) showed increased discharge during extension, suggesting phasic static gamma drive. There was no gamma drive associated with the late FDL alpha burst. In conclusion, the gamma drives to FHL and FDL differed during locomotion. FHL, which has the alpha drive of a classic extensor, received gamma drive that closely resembled other extensors. The gamma drive of FDL, which exhibits both extensor and flexor alpha synergies, did not match either muscle type. These observations are compatible with the view that fusimotor drive varies in different muscles during locomotion according to the prevailing sensorimotor requirements.
Topics: Animals; Cats; Decerebrate State; Electromyography; Female; Hindlimb; Male; Motor Activity; Muscle Spindles; Muscle, Skeletal; Neurons, Afferent; Stress, Mechanical; Toes
PubMed: 12154191
DOI: 10.1113/jphysiol.2001.013428