Activity patterns in individual hindlimb primary and secondary muscle spindle afferents during normal movements in unrestrained cats

1. Chronically implanted microelectrode wires in the L7 and S1 dorsal root ganglia were used to record unit activity from cat hindlimb primary and secondary muscle spindle afferents. Units could be reliably recorded for several days, permitting comparison of their activity with homonymous muscle EMG and length during a variety of normal, unrestrained movements. 2. The general observation was that among both primary and secondary endings there was a broad range of different patterns of activity depending on the type of muscle involved and the type of movement performed. 3. During walking, the activity of a given spindle primary was usually consistent among similar step cycles. However, the activity was usually poorly correlated with absolute muscle length, apparently unrealted to velocity of muscle stretch, and could change markedly for similar movements performed under different conditions. 4. Spindle activity modulation not apparently related to muscle length changes was assumed to be influenced by fusimotor activity. In certain muscles, this presumption leads to the conclusion that gamma-motoneurons may be activated out of phase with homonymous alpha-motoneurons as well as by more conventional alpha-gamma-motoneuron coactivation. 5. Simultaneous recordings of two spindle primary afferents from extensor digitorum longus indicated that spindles within the same muscle may differ considerably with respect to this presumed gamma-motoneuron drive. 6. Spindle secondary endings appeared to be predominantly passive indicators of muscle length during walking, but could demonstrate apparently strong fusimotor modulation during other motor activities such as postural changes and paw shaking. 7. Both primary and secondary endings were observed to undergo very rapid modulation of firing rates in response to presumed reflexly induced intrafusal contractions. 8. It is suggested that the pattern of fusimotor control of spindles may be tailored to the specific muscle and task being performed, rather than necessarily dominated by rigid alpha-gamma coactivation.

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Muscle spindles in human tibialis anterior encode muscle fascicle length changes

Journal of Neurophysiology ◽

10.1152/jn.00374.2016 ◽

2017 ◽

Vol 117 (4) ◽

pp. 1489-1498 ◽

Cited By ~ 19

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.

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Impulse rates and sensitivity to stretch of soleus muscle spindle afferent fibers during locomotion in premammillary cats

Journal of Neurophysiology ◽

10.1152/jn.1985.53.2.341 ◽

1985 ◽

Vol 53 (2) ◽

pp. 341-360 ◽

Cited By ~ 43

Author(s):

J. Taylor ◽

R. B. Stein ◽

P. R. Murphy

Keyword(s):

Muscle Spindle ◽

Soleus Muscle ◽

Muscle Afferents ◽

Emg Activity ◽

Step Cycle ◽

Muscle Spindle Afferents ◽

Large Length ◽

Length Changes ◽

Stretch Sensitivity ◽

Stimulation Of

Impulse from soleus muscle afferents were recorded in premammillary cats that were walking on a treadmill. In normal walking the effects of gamma-motoneurons on impulse rates of muscle spindle afferents are confounded by the effects of the large length changes that occur. To isolate the effects of gamma-motoneurons the leg was fixed in place for recording and denervated except for soleus muscle. Because gamma-motoneurons produce marked effects on the stretch sensitivity of muscle afferents, soleus muscle was oscillated about a present length so the stretch sensitivity of its afferents could be determined. The impulse rate of secondary muscle spindle afferents in soleus muscle was generally increased at all phases of the step cycle. The mean rate approximately doubled during walking (82 imp/s), compared with nonwalking (rest) periods (44 imp/s). The sensitivity to sinusoidal length changes was generally reduced throughout the step cycle (mean reduction = 33%). Primary muscle spindle afferents also showed an increased mean rate during walking (47 imp/s) compared with rest (24 imp/s). The impulse rate peaked after the muscle reached its maximum force and often showed a second peak before the maximum electromyogram (EMG) activity. The sensitivity to sinusoidal stretches varied cyclically during locomotion. During the extension phase it sometimes exceeded the resting value, but was greatly reduced during the flexion phase (mean reduction = 49% over whole cycle). Control experiments were carried out in which static and dynamic gamma-motoneurons were stimulated and activity from muscle spindle afferents was recorded in anesthetized cats. With the amplitude and frequency of stretch applied, stimulation of dynamic gamma-motoneurons usually increased and stimulation of static gamma-motoneurons usually decreased the sensitivity of primary muscle spindle afferents to sinusoidal stretch. The patterns observed in muscle spindle afferents suggest a strong, maintained activation of static gamma-motoneurons throughout the step cycle and a phasic activation of dynamic gamma-motoneurons, which is consistent with previous direct recordings from gamma-motoneurons. With this pattern of activating gamma-motoneurons, the secondary muscle spindle afferents will provide a good feedback signal of the large length changes that normally occur in the muscle during locomotion. The changes in sensitivity of primary muscle spindle afferents will complement central changes so the gain of the stretch reflex from extensors is high during extension (when required to help support the weight of the body) and low during flexion (when a high gain would be counterproductive).

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Characterization of Muscle Spindle Afferents in the Adult Mouse Using an In Vitro Muscle-Nerve Preparation

PLoS ONE ◽

10.1371/journal.pone.0039140 ◽

2012 ◽

Vol 7 (6) ◽

pp. e39140 ◽

Cited By ~ 15

Author(s):

Katherine A. Wilkinson ◽

Heidi E. Kloefkorn ◽

Shawn Hochman

Keyword(s):

Muscle Spindle ◽

Adult Mouse ◽

Muscle Spindle Afferents ◽

Muscle Nerve

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Projection of cat jaw muscle spindle afferents related to intrafusal fibre influence.

The Journal of Physiology ◽

10.1113/jphysiol.1993.sp019698 ◽

1993 ◽

Vol 465 (1) ◽

pp. 647-660 ◽

Cited By ~ 10

Author(s):

A Taylor ◽

R Durbaba ◽

J F Rodgers

Keyword(s):

Muscle Spindle ◽

Muscle Spindle Afferents ◽

Intrafusal Fibre ◽

Jaw Muscle

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Muscle dynamics in skipjack tuna: timing of red muscle shortening in relation to activation and body curvature during steady swimming

Journal of Experimental Biology ◽

10.1242/jeb.202.16.2139 ◽

1999 ◽

Vol 202 (16) ◽

pp. 2139-2150 ◽

Cited By ~ 18

Author(s):

R.E. Shadwick ◽

S.L. Katz ◽

K.E. Korsmeyer ◽

T. Knower ◽

J.W. Covell

Keyword(s):

Fork Length ◽

Muscle Length ◽

The Body ◽

Emg Activity ◽

Skipjack Tuna ◽

Force Transmission ◽

Muscle Strain ◽

Muscle Shortening ◽

Red Muscle ◽

Length Changes

Cyclic length changes in the internal red muscle of skipjack tuna (Katsuwonus pelamis) were measured using sonomicrometry while the fish swam in a water tunnel at steady speeds of 1.1-2.3 L s(−)(1), where L is fork length. These data were coupled with simultaneous electromyographic (EMG) recordings. The onset of EMG activity occurred at virtually the same phase of the strain cycle for muscle at axial locations between approximately 0.4L and 0.74L, where the majority of the internal red muscle is located. Furthermore, EMG activity always began during muscle lengthening, 40–50 prior to peak length, suggesting that force enhancement by stretching and net positive work probably occur in red muscle all along the body. Our results support the idea that positive contractile power is derived from all the aerobic swimming muscle in tunas, while force transmission is provided primarily by connective tissue structures, such as skin and tendons, rather than by muscles performing negative work. We also compared measured muscle length changes with midline curvature (as a potential index of muscle strain) calculated from synchronised video image analysis. Unlike contraction of the superficial red muscle in other fish, the shortening of internal red muscle in skipjack tuna substantially lags behind changes in the local midline curvature. The temporal separation of red muscle shortening and local curvature is so pronounced that, in the mid-body region, muscle shortening at each location is synchronous with midline curvature at locations that are 7–8 cm (i.e. 8–10 vertebral segments) more posterior. These results suggest that contraction of the internal red muscle causes deformation of the body at more posterior locations, rather than locally. This situation represents a unique departure from the model of a homogeneous bending beam, which describes red muscle strain in other fish during steady swimming, but is consistent with the idea that tunas produce thrust by motion of the caudal fin rather than by undulation of segments along the body.

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Electrical activity and relative length changes of dog limb muscles as a function of speed and gait

Journal of Experimental Biology ◽

10.1242/jeb.94.1.15 ◽

1981 ◽

Vol 94 (1) ◽

pp. 15-42 ◽

Cited By ~ 1

Author(s):

G. E. Goslow ◽

H. J. Seeherman ◽

C. R. Taylor ◽

M. N. McCutchin ◽

N. C. Heglund

Keyword(s):

Electrical Activity ◽

Stance Phase ◽

Biceps Brachii ◽

Vastus Lateralis ◽

Activity Patterns ◽

Relative Length ◽

Muscular Activity ◽

Triceps Brachii ◽

Limb Muscles ◽

Length Changes

Electrical activity and length changes of 11 muscles of the fore- and hind- limbs of dogs walking, running, and galloping on a treadmill, were measured as a function of forward speed and gait. Our purpose was to find out whether the activity patterns of the major limb muscles were consistent with the two mechanisms proposed for storage and recovery of energy within a stride: a ‘pendulum-like’ mechanism during a walk, and a ‘spring-like’ mechanism during a run. In the stance phase of the walking dog, we found that the supraspinatus, long head of the triceps brachii, biceps brachii, vastus lateralis, and gastrocnemius underwent only minor length changes during a relatively long portion of their activity, Thus, a major part of their activity during the walk seems consistent with a role in stabilization of the joints as the dog ‘pole-vaulted’ over its limbs (and thereby conserved energy). In the stance phase of trotting and/or galloping dogs, we found that the supraspinatus, lateral head of the triceps, vastus lateralis, and gastrocnemius were active while being stretched prior to shortening (as would be required for elastic storage of energy), and that this type of activity increased with increasing speed. We also found muscular activity in the select limb flexors that was consistent with storage of kinetic energy at the end of the swing phase and recovery during the propulsive stroke. This activity pattern was apparent in the latissimus dorsi during a walk and trot, and in the biceps femoris during a trot and gallop. We conclude that, during locomotion, a significant fraction of the electrical activity of a number of limbs muscles occurs while they undergo little or no length change or are being stretched prior to shortening and that these types of activities occur in a manner that would enable the operation of pendulum-like and spring-like mechanisms for conserving energy within a stride. Therefore these forms of muscular activity, in addition to the more familiar activity associated with muscle shortening, should be considered to be important during locomotion.

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