scholarly journals Changes in muscle spindle firing in response to length changes of neighboring muscles

2016 ◽  
Vol 115 (6) ◽  
pp. 3146-3155 ◽  
Author(s):  
Hiltsje A. Smilde ◽  
Jake A. Vincent ◽  
Guus C. Baan ◽  
Paul Nardelli ◽  
Johannes C. Lodder ◽  
...  

Skeletal muscle force can be transmitted to the skeleton, not only via its tendons of origin and insertion but also through connective tissues linking the muscle belly to surrounding structures. Through such epimuscular myofascial connections, length changes of a muscle may cause length changes within an adjacent muscle and hence, affect muscle spindles. The aim of the present study was to investigate the effects of epimuscular myofascial forces on feedback from muscle spindles in triceps surae muscles of the rat. We hypothesized that within an intact muscle compartment, muscle spindles not only signal length changes of the muscle in which they are located but can also sense length changes that occur as a result of changing the length of synergistic muscles. Action potentials from single afferents were measured intra-axonally in response to ramp-hold release (RHR) stretches of an agonistic muscle at different lengths of its synergist, as well as in response to synergist RHRs. A decrease in force threshold was found for both soleus (SO) and lateral gastrocnemius afferents, along with an increase in length threshold for SO afferents. In addition, muscle spindle firing could be evoked by RHRs of the synergistic muscle. We conclude that muscle spindles not only signal length changes of the muscle in which they are located but also local length changes that occur as a result of changing the length and relative position of synergistic muscles.

2017 ◽  
Vol 118 (3) ◽  
pp. 1677-1689 ◽  
Author(s):  
Michel Bernabei ◽  
Jaap H. van Dieën ◽  
Huub Maas

The aims of this study were to investigate changes 1) in the coordination of activation of the triceps surae muscle group, and 2) in muscle belly length of soleus (SO) and lateral gastrocnemius (LG) during locomotion (trotting) in response to increased stiffness of intermuscular connective tissues in the rat. We measured muscle activation and muscle belly lengths, as well as hindlimb kinematics, before and after an artificial enhancement of the connectivity between SO and LG muscles obtained by implanting a tissue-integrating surgical mesh at the muscles’ interface. We found that SO muscle activation decreased to 62%, while activation of LG and medial gastrocnemius muscles increased to 134 and 125%, respectively, compared with the levels measured preintervention. Although secondary additional or amplified activation bursts were observed with enhanced connectivity, the primary pattern of activation over the stride and the burst duration were not affected by the intervention. Similar muscle length changes after manipulation were observed, suggesting that length feedback from spindle receptors within SO and LG was not affected by the connectivity enhancement. We conclude that peripheral mechanical constraints given by morphological (re)organization of connective tissues linking synergists are taken into account by the central nervous system. The observed shift in activity toward the gastrocnemius muscles after the intervention suggests that these larger muscles are preferentially recruited when the soleus has a similar mechanical disadvantage in that it produces an unwanted flexion moment around the knee. NEW & NOTEWORTHY Connective tissue linkages between muscle-tendon units may act as an additional mechanical constraint on the musculoskeletal system, thereby reducing the spectrum of solutions for performing a motor task. We found that intermuscular coordination changes following intermuscular connectivity enhancement. Besides showing that the extent of such connectivity is taken into account by the central nervous system, our results suggest that recruitment of triceps surae muscles is governed by the moments produced at the ankle-knee joints.


1987 ◽  
Vol 57 (2) ◽  
pp. 574-595 ◽  
Author(s):  
S. E. Grill ◽  
W. Z. Rymer

The discharge of spindle afferents from medial gastrocnemius and soleus muscles was recorded in the decerebrated cat preparation, under isometric conditions and during ramp and hold stretches. Motor output was varied systematically by manual stimulation of the contralateral hindlimb. Twenty-six of 34 afferents showed response patterns consistent with enhancement of dynamic and/or static fusimotor input with increasing muscle force. To establish whether force-related fusimotor effects were mediated at least partly by beta-input, beta-innervation to these same spindles was sought, using a ventral root stimulation protocol. Twenty-three of the 34 afferents were shown to receive beta-innervation, which was most often static in type. For two measures of fusimotor action, the slope of the afferent dynamic rate-length relation and the discharge rate measured during the last portion of ramp stretch, significant increases in the measure, which paralleled increases in muscle force, made it statistically more likely that the afferent received beta-innervation. Our measures did not successfully predict the type of beta-input (beta-static or beta-dynamic). Procaine block of gamma-fibers produced substantial reductions in fusimotor effect in seven spindle afferents (although modest residual fusimotor effects were detectable for 3/7 afferents). The severity of these reductions indicates that beta-action probably requires concurrent gamma-input to the spindle in order to be effective. In support of this possibility, the fusimotor effects of electrical stimulation of single beta-fibers were greatly reduced for five out of six afferents during procaine block of gamma-fibers, compared with the beta-effects recorded when modest levels of spontaneous gamma-activity were present. We conclude that beta-innervation to muscle spindles of triceps surae is common and that this innervation exerts significant fusimotor effects. It appears likely that beta-motoneurons are able to produce both static and dynamic effects above extrafusal threshold, but that the actions require on-going gamma-activity in order to be effective.


2018 ◽  
Vol 120 (5) ◽  
pp. 2484-2497 ◽  
Author(s):  
William P. Mayer ◽  
Andrew J. Murray ◽  
Susan Brenner-Morton ◽  
Thomas M. Jessell ◽  
Warren G. Tourtellotte ◽  
...  

Terrestrial animals increase their walking speed by increasing the activity of the extensor muscles. However, the mechanism underlying how this speed-dependent amplitude modulation is achieved remains obscure. Previous studies have shown that group Ib afferent feedback from Golgi tendon organs that signal force is one of the major regulators of the strength of muscle activity during walking in cats and humans. In contrast, the contribution of group Ia/II afferent feedback from muscle spindle stretch receptors that signal angular displacement of leg joints is unclear. Some studies indicate that group II afferent feedback may be important for amplitude regulation in humans, but the role of muscle spindle feedback in regulation of muscle activity strength in quadrupedal animals is very poorly understood. To examine the role of feedback from muscle spindles, we combined in vivo electrophysiology and motion analysis with mouse genetics and gene delivery with adeno-associated virus. We provide evidence that proprioceptive sensory feedback from muscle spindles is important for the regulation of the muscle activity strength and speed-dependent amplitude modulation. Furthermore, our data suggest that feedback from the muscle spindles of the ankle extensor muscles, the triceps surae, is the main source for this mechanism. In contrast, muscle spindle feedback from the knee extensor muscles, the quadriceps femoris, has no influence on speed-dependent amplitude modulation. We provide evidence that proprioceptive feedback from ankle extensor muscles is critical for regulating muscle activity strength as gait speed increases. NEW & NOTEWORTHY Animals upregulate the activity of extensor muscles to increase their walking speed, but the mechanism behind this is not known. We show that this speed-dependent amplitude modulation requires proprioceptive sensory feedback from muscle spindles of ankle extensor muscle. In the absence of muscle spindle feedback, animals cannot walk at higher speeds as they can when muscle spindle feedback is present.


2004 ◽  
Vol 91 (5) ◽  
pp. 2164-2171 ◽  
Author(s):  
Valerie K. Haftel ◽  
Edyta K. Bichler ◽  
T. Richard Nichols ◽  
Martin J. Pinter ◽  
Timothy C. Cope

Among the mechanisms that may result in modulation of the stretch reflex by the recent history of muscle contraction is the history dependence observed under some conditions in the response properties of muscle spindles. The present study was designed to test one report that in successive trials of muscle stretch-release, spindle afferent firing during stretch, i.e., the dynamic response shows no history dependence beyond the initial burst of firing at stretch onset. Firing responses of spindle afferents were recorded during sets of three consecutive trials of triangular stretch-release applied to triceps surae muscles in barbiturate-anesthetized rats. All 69 spindle afferents fired more action potentials (spikes) during the dynamic response of the first trial, excluding the initial burst, than in the following two trials. The reduced dynamic response (RDR) was nearly complete after trial 1 and amounted to an average of ∼12 fewer spikes (16 pps slower firing rate) in trial 3 than in trial 1. RDR was sensitive to the interval between stretch sets but independent of stretch velocity (4–32 mm/s). RDR was reflected in the synaptic potentials recorded intracellularly from 16 triceps surae α-motoneurons: depolarization during muscle stretch was appreciably reduced after trial 1. These findings demonstrate history dependence of spindle afferent responses that extends throughout the dynamic response in successive muscle stretches and that is synaptically transmitted to motoneurons with the probable effect, unless otherwise compensated, of modulating the stretch reflex.


1998 ◽  
Vol 79 (5) ◽  
pp. 2265-2276 ◽  
Author(s):  
Sabine M. P. Verschueren ◽  
Paul J. Cordo ◽  
Stephan P. Swinnen

Verschueren, Sabine M. P., Paul J. Cordo, and Stephan P. Swinnen. Representation of wrist joint kinematics by the ensemble of muscle spindles from synergistic muscles. J. Neurophysiol. 79: 2265–2276, 1998. Proprioceptive information about movement is transmitted to the central nervous system by a variety of receptor types, which are widely distributed among the muscles, joints, and skin. Muscle spindles are known to be an important and reliable source of information for the perception of movement kinematics. Previous studies that focused on the characteristics of single muscle spindle firing patterns have left the impression that each receptor fires in relation to a number of kinematic variables, leaving the following question unanswered: what role is played by the ensemble of muscle spindles within the same muscle or within synergistic muscles? The study described in this paper addressed whether the perception of joint position and velocity is based on the net input of muscle spindles residing in all synergistic muscles crossing a joint. Normal human adults performed a motor coordination task that required perception of joint velocity and dynamic position at the wrist. The task was to open the left hand briskly as the right wrist was passively rotated in the flexion direction through a prescribed target angle. In randomly occurring trials, the tendons to three muscles [extensor carpi radialis (ECR), extensor carpi ulnaris (ECU), and extensor digitorum (ED)] were vibrated either individually or in different combinations during the performance of the motor task. Tendon vibration is known to distort muscle spindle firing patterns, and consequently, kinesthesia. By comparing performance errors with and without tendon vibration, the relative influences of muscle spindles residing in ECR, ECU, and ED were quantified. Vibration of the individual ECR, ECU, or ED tendons produced systematic undershoot errors in performance, consistent with the misperception of wrist velocity and dynamic position. Performance errors were larger when combinations of, rather than individual, muscle tendons were vibrated. The error resulting from simultaneous vibration of ECR and ECU was roughly equal to the sum of the errors produced by vibration of the individual tendons. These effects of vibrating synergistic tendons at the wrist suggest that kinesthesia is derived from the integrated input of muscle spindles from all synergistic muscles.


2017 ◽  
Vol 117 (4) ◽  
pp. 1489-1498 ◽  
Author(s):  
James Day ◽  
Leah R. Bent ◽  
Ingvars Birznieks ◽  
Vaughan G. Macefield ◽  
Andrew G. Cresswell

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.


2011 ◽  
Vol 110 (3) ◽  
pp. 627-637 ◽  
Author(s):  
A. J. Bergquist ◽  
J. M. Clair ◽  
D. F. Collins

Neuromuscular electrical stimulation (NMES) can be delivered over a nerve trunk or muscle belly and can generate contractions by activating motor (peripheral pathway) and sensory (central pathway) axons. In the present experiments, we compared the peripheral and central contributions to plantar flexion contractions evoked by stimulation over the tibial nerve vs. the triceps surae muscles. Generating contractions through central pathways follows Henneman's size principle, whereby low-threshold motor units are activated first, and this may have advantages for rehabilitation. Statistical analyses were performed on data from trials in which NMES was delivered to evoke 10–30% maximum voluntary torque 2–3 s into the stimulation (Time1). Two patterns of stimulation were delivered: 1) 20 Hz for 8 s; and 2) 20–100-20 Hz for 3–2-3 s. Torque and soleus electromyography were quantified at the beginning (Time1) and end (Time2; 6–7 s into the stimulation) of each stimulation train. H reflexes (central pathway) and M waves (peripheral pathway) were quantified. Motor unit activity that was not time-locked to each stimulation pulse as an M wave or H reflex (“asynchronous” activity) was also quantified as a second measure of central recruitment. Torque was not different for stimulation over the nerve or the muscle. In contrast, M waves were approximately five to six times smaller, and H reflexes were approximately two to three times larger during NMES over the nerve vs. the muscle. Asynchronous activity increased by 50% over time, regardless of the stimulation location or pattern, and was largest during NMES over the muscle belly. Compared with NMES over the triceps surae muscles, NMES over the tibial nerve produced contractions with a relatively greater central contribution, and this may help reduce muscle atrophy and fatigue when NMES is used for rehabilitation.


1999 ◽  
Vol 23 (5) ◽  
pp. 436-439 ◽  
Author(s):  
Dietmar Rafolt ◽  
Eugen Gallasch ◽  
Winfried Mayr ◽  
Hermann Lanmuller

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