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Muscle Spindles: Their Messages and Their Fusimotor Supply

Peter B. C. Matthews

10.1002/cphy.cp010206

Source: Supplement 2: Handbook of Physiology, The Nervous System, Motor Control

Originally published: 1981

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Tendon Organs
2 Structure of Muscle Spindles
2.1 Classic View
2.2 Recognition of Motor Duality
2.3 Subdivision of Nuclear‐Bag Fibers
3 Functional Properties of Primary and Secondary Spindle Afferent Endings
3.1 Different Responses to Various Stimuli
3.2 Mode of Summation of Signal Components
3.3 Amplitude Nonlinearity
3.4 Linear Responses to Sinusoidal Stretching
3.5 Assessment
3.6 Possible Intermediate Endings
4 Motor Supply to Muscle Spindle
4.1 Gamma Motor Axons
4.2 Delimitation of Static and Dynamic Fusimotor Axons
4.3 Intrafusal Destination of Static and Dynamic Axons
4.4 Properties of Intrafusal Muscle Fibers
4.5 Beta or Skeletofusimotor Axons
5 Possible Functional Roles for the Fusimotor System
5.1 Maintenance of Sensitivity
5.2 Central Regulation of Spindle Sensitivity (Parameter Control)
5.3 Fusimotor Biasing and Suggested Role as Servo Input
5.4 Assessment
6 Summary
6.1 Structure
6.2 Functional Differences Between Primary and Secondary Endings
6.3 Static and Dynamic Fusimotor Axons
6.4 Possible Functional Roles for the Fusimotor System
Figure 1. Figure 1.

Classic picture of muscle spindle as seen by Ruffini in 1898 161. Retouched.
Figure 2. Figure 2.

Simplified diagram of central region of muscle spindle as it was recognized in 1964, largely on the basis of Boyd's work 30, with 2 types of intrafusal muscle fiber, each with its own motor innervation, and 2 kinds of afferent axon.

From Matthews 137
Figure 3. Figure 3.

Contrasting responses of spindle primary and secondary endings of cat to a rapidly applied stretch to the soleus (approximately 14 mm at 70 mm/s). Responses shown in both presence and absence of tonic fusimotor activity of decerebrate cat. Bottom, responses of endings when deefferented by ventral root (V.R.) section. Top, responses of the same endings when ventral roots were intact and were tonically biased by spontaneous fusimotor activity.

From Matthews 137
Figure 4. Figure 4.

Diagrammatic comparison of responses of “typical” primary and secondary endings to various stimuli of large amplitude applied in the absence of fusimotor activity.

From Matthews 135
Figure 5. Figure 5.

Effect of increasing the velocity of stretching on the initial burst given by a primary ending at beginning of stretch and on the more prolonged velocity response. A 6‐mm stretch was applied to a deefferented soleus muscle of cat. Time calibration applies only to the static phases of the response; dynamic phases are on slightly expanded time scales, which may be deduced from the parameters of stretching.

From Matthews 137
Figure 6. Figure 6.

Comparison of the sensitivity to sinusoidal stretching within the linear range of a primary and a secondary ending studied together over a wide range of frequencies of stretching measured in cycles per second (Hz). The sensitivity at any frequency is defined as the amplitude of the afferent response, considered as a sinusoidal modulation of firing (measured in impulses per second) divided by the amplitude of stretching (measured in millimeters). The endings were being tonically biased by the spontaneous fusimotor activity of the decerebrate cat. The continuous lines represent the vector sum of responses to the length component of the stimulus (dominant for the horizontal portion at low frequencies) and to the velocity component (dominant for the diagonal portion of the line at high frequencies). The same curve transposed vertically approximately fits both endings over a considerable region. This shows that in the linear range they differ in their absolute sensitivity, rather than in the ratio of their length to their velocity sensitivity. The upward deviation of the points for the primary ending above 10–20 Hz can be taken as showing an “acceleration sensitivity,” but at these frequencies the linear range is only a few μm in extent so the finding cannot be transferred to stretches of appreciable extent. As a very rough approximation the linear range at any frequency can be deduced from the graphs by assuming that it correponds to a modulation of firing of some 15 impulses/s, so that at 1 c/s it was around 150 μm for the primary and 2 mm for the secondary ending.

From Matthews and Stein 138
Figure 7. Figure 7.

Soleus muscle of decerebrate cat contracting in response to stimulation of contralateral peroneal nerve. Physiological manifestation of a high sensitivity of primary ending, but not of secondary ending, to small stretches. Sensitivity of primary ending is demonstrated by the fact that both of the 2 primary endings can be seen to respond in synchrony to the small irregularities occurring in a reflexly induced muscle contraction, which occurred under approximately isotonic conditions. Discharges of the 3 afferents were recorded simultaneously.

From Matthews 137
Figure 8. Figure 8.

Contrasting effects of static (γS) and dynamic (γD) fusimotor axons on responsiveness of a primary ending to large amplitude ramp stretching in cat. Records of instantaneous frequency, a, in absence of fusimotor stimulation; b, during repetitive static axon stimulation; c, during repetitive dynamic axon stimulation. Stretch was 6 mm at 30 mm/s. Time scale expanded during dynamic phase of stretch.

From Brown and Matthews 42
Figure 9. Figure 9.

Simultaneous stimulation of a pair of single fusimotor axons (1 static, γS; 1 dynamic, γD), of cat. Each axon stimulated at several frequencies to show effect on responsiveness of a primary ending to a ramp stretch as the balance between them is shifted.

From Emonet‐Dénand, Matthews, et al. 78
Figure 10. Figure 10.

Developing views on relation between functional classification into static (γS) and dynamic (γD) axons, and morphological classification of intrafusal muscle fibers. Dotted line from static axon to bag1 fiber represents the chief matter of current controversy.
Figure 11. Figure 11.

Drawing of the way in which a sole surviving static axon following degeneration of the rest of the motor innervation in cat was seen to distribute itself between a bag fiber and 2 chain fibers. All the terminations are trail‐type ending.

From Barker et al. 19
Figure 12. Figure 12.

Examples from the first study of the intrafusal depletion of glycogen after stimulation of single γ‐fibers. Static axon, γS; dynamic axon, γD. Each horizontal row represents a spindle, with its several intrafusal muscle fibers shown by circles. Presence of glycogen is shown by solid circle, and its depletion following neural activation of the fiber is shown by open circle. The bag fibers were not then subdivided.

Rearranged from Brown and Butler 35
Figure 13. Figure 13.

Recent examples that glycogen depletion, after stimulation of single dynamic axons, is restricted to bag1 intrafusal fibers. Each row represents a spindle with its intrafusal muscle fibers shown by circles. Solid circle, glycogen presence; open circle, glycogen depletion.

Adapted from Barker et al. 17
Figure 14. Figure 14.

Diagrammatic representation of the particular intrafusal muscle fibers that were seen to contract by Boyd and his colleagues in isolated spindles after stimulation of single fusimotor axons. Each row represents a spindle and each symbol represents an intrafusal muscle fiber that was seen to move with fusimotor stimulation. The symbol is varied with the type of axon that was found to activate the fiber in question. •, Dynamic γ; ○, dynamic β; △, static γ. When a given axon influenced 2 different types of intrafusal fiber the symbols are joined by a horizontal line. It may be seen that a bag fiber influenced by a dynamic axon (dynamic nuclear bag) was never influenced by a static axon or in combination with a chain fiber, but that other bag fibers were activated by static axons (static nuclear bag) and that this was commonly in conjunction with chain activation.

Adapted from Boyd et al. 32
Figure 15. Figure 15.

Motor innervation of spindle as described by Boyd et al. in 1977 with a completely independent innervation of bag1 and bag2 intrafusal muscle fibers, but with the innervation of bag2 and chain fibers partly in common.

Redrawn from Boyd et al. 32
Figure 16. Figure 16.

Recent examples of varied patterns ot glycogen depletion involving all 3 types of intrafusal fiber seen when single static axons are stimulated. Each row represents a spindle with its intrafusal muscle fibers shown by circles. Solid circle, glycogen presence; open circle, glycogen depletion.

Adapted from Barker et al. 17
Figure 17. Figure 17.

Position response of a primary ending as seen during dynamic stretching, assuming that length and velocity components of response are approximately additive. Dynamic fusimotor (γD) stimulation appears to have a specific action in augmenting this dynamically determined position response without appreciably affecting the position response determined under truly static conditions; the latter then has a much lower value than the former.

Redrawn from Crowe and Matthews 62
Figure 18. Figure 18.

Effects of fusimotor stimulation on the relation for a primary ending between dynamic index and velocity of stretching for large amplitude stretching (6‐mm stretch of cat soleus). Dynamic index is difference between frequency of discharge just before end of dynamic phase of a ramp stretch and that occurring 0.5 s later with the muscle held at the final length.

From Crowe and Matthews 62
Figure 19. Figure 19.

Change induced by fusimotor stimulation in responsiveness of spindle primary ending to small amplitude sinusoidal stretching of a wide range of frequencies. Top, logarithmic plots of ratio of sensitivity of activated spindle (cf. Fig. 6) to that of passive spindle. Bottom, linear plots of arithmetic difference between the phases in the 2 states. For motor control purposes, only the effects below 20–30 Hz appear relevant. At each frequency the amplitude of stretching was restricted to the linear range. ○, Obtained from a single spindle; •, static and dynamic effects from separate spindles.

From Goodwin, Hulliger, and Matthews 82
Figure 20. Figure 20.

Effect of fusimotor stimulation on response of a primary ending to sinusoidal stretching of appreciable amplitude (1 mm peak to peak at 3 Hz.) γD, Dynamic axon; γS, static axon.

From Crowe and Matthews 63
Figure 21. Figure 21.

Discharge in the human of a presumed primary spindle afferent during a weak, voluntary isometric contraction of the muscle it supplied (flexor of index finger). EMG, electromyogram.

From Vallbo 179
Figure 22. Figure 22.

Responses of a presumed spindle primary afferent from a jaw closing muscle of conscious cat. A: during eating. B: during lapping. Top, spindle spikes; middle, jaw movement with jaw opening upward, length of arrow indicates 25°; bottom, gross electromyogram recorded from masseter muscle in which the spindle lay.

From Cody et al. 55
Figure 23. Figure 23.

Example of a period of movement in the conscious cat. Degree of fusimotor activity was such that the discharge of a presumed spindle primary afferent remained approximately constant. Records taken during licking of lips from a jaw‐closing spindle that behaved similarly to that of Figure 22A. Length of arrow indicates 25°.

From Cody et al. 55
Figure 24. Figure 24.

Behavior of a presumed primary spindle afferent in the human during slow rhythmic voluntary movement. Spindle lay in the tibialis anterior. A: foot was moved passively. B‐D: foot was moved actively either unloaded or against a load (expressed as torque in Newton meters) produced by a rubber band opposing flexion, and thus augmenting contraction of the tibialis anterior. Top, instantaneous frequency of firing; bottom, ankle movement.

From Burke et al. 46
Figure 25. Figure 25.

Summarizing diagram of static (γS) and dynamic (γD) fusimotor actions that may be currently deemed to be of functional importance.


Figure 1.

Classic picture of muscle spindle as seen by Ruffini in 1898 161. Retouched.



Figure 2.

Simplified diagram of central region of muscle spindle as it was recognized in 1964, largely on the basis of Boyd's work 30, with 2 types of intrafusal muscle fiber, each with its own motor innervation, and 2 kinds of afferent axon.

From Matthews 137


Figure 3.

Contrasting responses of spindle primary and secondary endings of cat to a rapidly applied stretch to the soleus (approximately 14 mm at 70 mm/s). Responses shown in both presence and absence of tonic fusimotor activity of decerebrate cat. Bottom, responses of endings when deefferented by ventral root (V.R.) section. Top, responses of the same endings when ventral roots were intact and were tonically biased by spontaneous fusimotor activity.

From Matthews 137


Figure 4.

Diagrammatic comparison of responses of “typical” primary and secondary endings to various stimuli of large amplitude applied in the absence of fusimotor activity.

From Matthews 135


Figure 5.

Effect of increasing the velocity of stretching on the initial burst given by a primary ending at beginning of stretch and on the more prolonged velocity response. A 6‐mm stretch was applied to a deefferented soleus muscle of cat. Time calibration applies only to the static phases of the response; dynamic phases are on slightly expanded time scales, which may be deduced from the parameters of stretching.

From Matthews 137


Figure 6.

Comparison of the sensitivity to sinusoidal stretching within the linear range of a primary and a secondary ending studied together over a wide range of frequencies of stretching measured in cycles per second (Hz). The sensitivity at any frequency is defined as the amplitude of the afferent response, considered as a sinusoidal modulation of firing (measured in impulses per second) divided by the amplitude of stretching (measured in millimeters). The endings were being tonically biased by the spontaneous fusimotor activity of the decerebrate cat. The continuous lines represent the vector sum of responses to the length component of the stimulus (dominant for the horizontal portion at low frequencies) and to the velocity component (dominant for the diagonal portion of the line at high frequencies). The same curve transposed vertically approximately fits both endings over a considerable region. This shows that in the linear range they differ in their absolute sensitivity, rather than in the ratio of their length to their velocity sensitivity. The upward deviation of the points for the primary ending above 10–20 Hz can be taken as showing an “acceleration sensitivity,” but at these frequencies the linear range is only a few μm in extent so the finding cannot be transferred to stretches of appreciable extent. As a very rough approximation the linear range at any frequency can be deduced from the graphs by assuming that it correponds to a modulation of firing of some 15 impulses/s, so that at 1 c/s it was around 150 μm for the primary and 2 mm for the secondary ending.

From Matthews and Stein 138


Figure 7.

Soleus muscle of decerebrate cat contracting in response to stimulation of contralateral peroneal nerve. Physiological manifestation of a high sensitivity of primary ending, but not of secondary ending, to small stretches. Sensitivity of primary ending is demonstrated by the fact that both of the 2 primary endings can be seen to respond in synchrony to the small irregularities occurring in a reflexly induced muscle contraction, which occurred under approximately isotonic conditions. Discharges of the 3 afferents were recorded simultaneously.

From Matthews 137


Figure 8.

Contrasting effects of static (γS) and dynamic (γD) fusimotor axons on responsiveness of a primary ending to large amplitude ramp stretching in cat. Records of instantaneous frequency, a, in absence of fusimotor stimulation; b, during repetitive static axon stimulation; c, during repetitive dynamic axon stimulation. Stretch was 6 mm at 30 mm/s. Time scale expanded during dynamic phase of stretch.

From Brown and Matthews 42


Figure 9.

Simultaneous stimulation of a pair of single fusimotor axons (1 static, γS; 1 dynamic, γD), of cat. Each axon stimulated at several frequencies to show effect on responsiveness of a primary ending to a ramp stretch as the balance between them is shifted.

From Emonet‐Dénand, Matthews, et al. 78


Figure 10.

Developing views on relation between functional classification into static (γS) and dynamic (γD) axons, and morphological classification of intrafusal muscle fibers. Dotted line from static axon to bag1 fiber represents the chief matter of current controversy.



Figure 11.

Drawing of the way in which a sole surviving static axon following degeneration of the rest of the motor innervation in cat was seen to distribute itself between a bag fiber and 2 chain fibers. All the terminations are trail‐type ending.

From Barker et al. 19


Figure 12.

Examples from the first study of the intrafusal depletion of glycogen after stimulation of single γ‐fibers. Static axon, γS; dynamic axon, γD. Each horizontal row represents a spindle, with its several intrafusal muscle fibers shown by circles. Presence of glycogen is shown by solid circle, and its depletion following neural activation of the fiber is shown by open circle. The bag fibers were not then subdivided.

Rearranged from Brown and Butler 35


Figure 13.

Recent examples that glycogen depletion, after stimulation of single dynamic axons, is restricted to bag1 intrafusal fibers. Each row represents a spindle with its intrafusal muscle fibers shown by circles. Solid circle, glycogen presence; open circle, glycogen depletion.

Adapted from Barker et al. 17


Figure 14.

Diagrammatic representation of the particular intrafusal muscle fibers that were seen to contract by Boyd and his colleagues in isolated spindles after stimulation of single fusimotor axons. Each row represents a spindle and each symbol represents an intrafusal muscle fiber that was seen to move with fusimotor stimulation. The symbol is varied with the type of axon that was found to activate the fiber in question. •, Dynamic γ; ○, dynamic β; △, static γ. When a given axon influenced 2 different types of intrafusal fiber the symbols are joined by a horizontal line. It may be seen that a bag fiber influenced by a dynamic axon (dynamic nuclear bag) was never influenced by a static axon or in combination with a chain fiber, but that other bag fibers were activated by static axons (static nuclear bag) and that this was commonly in conjunction with chain activation.

Adapted from Boyd et al. 32


Figure 15.

Motor innervation of spindle as described by Boyd et al. in 1977 with a completely independent innervation of bag1 and bag2 intrafusal muscle fibers, but with the innervation of bag2 and chain fibers partly in common.

Redrawn from Boyd et al. 32


Figure 16.

Recent examples of varied patterns ot glycogen depletion involving all 3 types of intrafusal fiber seen when single static axons are stimulated. Each row represents a spindle with its intrafusal muscle fibers shown by circles. Solid circle, glycogen presence; open circle, glycogen depletion.

Adapted from Barker et al. 17


Figure 17.

Position response of a primary ending as seen during dynamic stretching, assuming that length and velocity components of response are approximately additive. Dynamic fusimotor (γD) stimulation appears to have a specific action in augmenting this dynamically determined position response without appreciably affecting the position response determined under truly static conditions; the latter then has a much lower value than the former.

Redrawn from Crowe and Matthews 62


Figure 18.

Effects of fusimotor stimulation on the relation for a primary ending between dynamic index and velocity of stretching for large amplitude stretching (6‐mm stretch of cat soleus). Dynamic index is difference between frequency of discharge just before end of dynamic phase of a ramp stretch and that occurring 0.5 s later with the muscle held at the final length.

From Crowe and Matthews 62


Figure 19.

Change induced by fusimotor stimulation in responsiveness of spindle primary ending to small amplitude sinusoidal stretching of a wide range of frequencies. Top, logarithmic plots of ratio of sensitivity of activated spindle (cf. Fig. 6) to that of passive spindle. Bottom, linear plots of arithmetic difference between the phases in the 2 states. For motor control purposes, only the effects below 20–30 Hz appear relevant. At each frequency the amplitude of stretching was restricted to the linear range. ○, Obtained from a single spindle; •, static and dynamic effects from separate spindles.

From Goodwin, Hulliger, and Matthews 82


Figure 20.

Effect of fusimotor stimulation on response of a primary ending to sinusoidal stretching of appreciable amplitude (1 mm peak to peak at 3 Hz.) γD, Dynamic axon; γS, static axon.

From Crowe and Matthews 63


Figure 21.

Discharge in the human of a presumed primary spindle afferent during a weak, voluntary isometric contraction of the muscle it supplied (flexor of index finger). EMG, electromyogram.

From Vallbo 179


Figure 22.

Responses of a presumed spindle primary afferent from a jaw closing muscle of conscious cat. A: during eating. B: during lapping. Top, spindle spikes; middle, jaw movement with jaw opening upward, length of arrow indicates 25°; bottom, gross electromyogram recorded from masseter muscle in which the spindle lay.

From Cody et al. 55


Figure 23.

Example of a period of movement in the conscious cat. Degree of fusimotor activity was such that the discharge of a presumed spindle primary afferent remained approximately constant. Records taken during licking of lips from a jaw‐closing spindle that behaved similarly to that of Figure 22A. Length of arrow indicates 25°.

From Cody et al. 55


Figure 24.

Behavior of a presumed primary spindle afferent in the human during slow rhythmic voluntary movement. Spindle lay in the tibialis anterior. A: foot was moved passively. B‐D: foot was moved actively either unloaded or against a load (expressed as torque in Newton meters) produced by a rubber band opposing flexion, and thus augmenting contraction of the tibialis anterior. Top, instantaneous frequency of firing; bottom, ankle movement.

From Burke et al. 46


Figure 25.

Summarizing diagram of static (γS) and dynamic (γD) fusimotor actions that may be currently deemed to be of functional importance.

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Article Title: Muscle Spindles: Their Messages and Their Fusimotor Supply
 

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Peter B. C. Matthews. Muscle Spindles: Their Messages and Their Fusimotor Supply. Compr Physiol 2011, Supplement 2: Handbook of Physiology, The Nervous System, Motor Control: 189-228. First published in print 1981. doi: 10.1002/cphy.cp010206