Comprehensive Physiology Wiley Online Library

Muscle Spindles: Their Messages and Their Fusimotor Supply

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. BD: 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. BD: 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.

References
 1. Adal, M. N., and D. Barker. Intramuscular branching of fusimotor fibres. J. Physiol. London, 177: 288–299, 1965.
 2. Anderson, J. H. Dynamic characteristics of Golgi tendon organs. Brain Res., 67: 531–537, 1974.
 3. Andersson, B. F., G. Lennerstrand, and U. Thoden. Response characteristics of muscle spindle endings at constant length to variations in fusimotor activation. Acta Physiol. Scand., 74: 301–318, 1968.
 4. Andrew, B. L., G. C. Leslie, and N. J. Part. Some observations on the efferent innervation of rat soleus muscle spindles. Exp. Brain Res., 31: 433–443, 1978.
 5. Andrew, B. L., and N. J. Part. The division of control of muscle spindles between fusimotor and mixed skeletomotor fibres in a rat caudal muscle. Q. J. Exp. Physiol., 57: 213–225, 1974.
 6. Appelberg, B., P. Bessou, and Y. Laporte. Action of static and dynamic fusimotor fibres on secondary endings of cat's spindles. J. Physiol. London, 185: 160–171, 1966.
 7. Appelberg, B., and A. Molander. A rubro‐olivary pathway. I. Identification of a descending system for control of dynamic sensitivity of muscle spindles. Exp. Brain Res., 3: 372–381, 1967.
 8. Arbuthnott, E. R., I. A. Boyd, M. H. Gladden, and P. N. McWilliam. Real and apparent γ axon contraction sites in intrafusal fibres. J. Physiol. London 268: 25P–26P, 1977.
 9. Banks, R. W., D. Barker, P. Bessou, B. Pages, and M. J. Stacey. Serial‐section analysis of cat muscle spindles following observation of the effects of stimulating dynamic fusimotor axons. J. Physiol. London 263: 180P–181P, 1976.
 10. Banks, R. W., D. Barker, P. Bessou, B. Pages, and M. J. Stacey. Histological analysis of muscle spindles following direct observation of effects of stimulating dynamic and static motor axons. J. Physiol. London, 283: 605–619, 1978.
 11. Banks, R. W., D. Barker, and M. J. Stacey. Intrafusal branching and distribution of primary and secondary afferents. J. Physiol. London 272: 66P–67P, 1977.
 12. Banks, R. W., D. W. Harker, and M. J. Stacey. A study of mammalian intrafusal muscle fibres using a combined histo‐chemical and ultrastructural approach. J. Anat., 123: 783–796, 1977.
 13. Barker, D. The innervation of the muscle spindle. Q. J. Microsc. Sci., 89: 143–186, 1948.
 14. Barker, D. (editor). Symposium on Muscle Receptors. Proceedings. Hong Kong: Hong Kong Univ. Press, 1962.
 15. Barker, D. The morphology of muscle receptors. In: Handbook of Sensory Physiology. Muscle Receptors, edited by C. C. Hunt. Berlin: Springer‐Verlag, 1974, vol. 3, pt. 2, p. 1–190.
 16. Barker, D., P. Bessou, E. Jankowska, B. Pagès, and M. J. Stacey. Identification of intrafusal muscle fibres activated by single fusimotor axons and injected with fluorescent dye in cat tenuissimus spindles. J. Physiol. London, 275: 149–165, 1978.
 17. Barker, D., F. Emonet‐Dénand, D. W. Harker, L. Jami, and Y. Laporte. Distribution of fusimotor axons to intrafusal muscle fibres in cat tenuissimus spindles as determined by the glycogen‐depletion method. J. Physiol. London, 261: 49–69, 1976.
 18. Barker, D., F. Emonet‐Dénand, D. W. Harker, L. Jami, and Y. Laporte. Types of intra‐ and extrafusal muscle fibre innervated by dynamic skeletofusimotor axons in cat peroneus brevis and tenuissimus muscles, as determined by the glycogen depletion method. J. Physiol. London, 266: 713–726, 1977.
 19. Barker, D., F. Emonet‐Dénand, Y. Laporte, U. Proske, and D. W. Stacey. Morphological identification and intrafusal distribution of the endings of static fusimotor axons in the cat. J. Physiol. London, 230: 405–427, 1973.
 20. Barker, D., and M. C. Ip. The motor innervation of cat and rabbit muscle spindles. J. Physiol. London 171: 27P–28P, 1965.
 21. Barker, D., and D. W. Stacey. Rabbit intrafusal muscle fibres. J. Physiol. London 210: 70P–72P, 1970.
 22. Barker, D., M. J. Stacey, and M. N. Adal. Fusimotor innervation in the cat. Philos. Trans. R. Soc. London Ser. B., 258: 315–346, 1970.
 23. Bessou, P., F. Emonet‐Dénand, and Y. Laporte. Motor fibres innervating extrafusal and intrafusal muscle fibres in the cat. J. Physiol. London, 180: 469–672, 1965.
 24. Bessou, P., and Y. Laporte. Potentials fusoriaux provoqués par Ia stimulation de fibres fusimotrices chez le chat. C. R. Acad. Sci., 260: 4827–4830, 1965.
 25. Bessou, P., Y. Laporte, and B. Pagès. Frequencygrams of spindle primary endings elicited by stimulation of static and dynamic fusimotor fibres. J. Physiol. London, 196: 47–63, 1968.
 26. Bessou, P., and B. Pagès. Intracellular potentials from intrafusal muscle fibres evoked by stimulation of static and dynamic fusimotor axons in the cat. J. Physiol. London, 227: 709–727, 1972.
 27. Bessou, P., and B. Pagès. Cinematographic analysis of contractile events produced in intrafusal muscle fibres by stimulation of static and dynamic fusimotor axons. J. Physiol. London, 252: 397–427, 1975.
 28. Bianconi, R., and J. P. Van Der Meulen. The response to vibration of the end organs of mammalian muscle spindles. J. Neurophysiol., 26: 177–190, 1963.
 29. Binder, M. D., J. S. Kronin, G. P. Moore, and D. G. Stuart. The response of Golgi tendon organs to single motor unit contractions. J. Physiol. London, 271: 337–349, 1977.
 30. Boyd, I. A. The structure and innervation of the nuclear bag muscle fibres and the nuclear chain muscle fibre system in mammalian muscle spindles. Philos. Trans. R. Soc. London Ser. B., 245: 81–136, 1962.
 31. Boyd, I. A. The response of fast and slow nuclear bag fibres and nuclear chain fibres in isolated cat muscle spindles to fusimotor stimulation, and the effect of intrafusal contraction on the sensory endings. Q. J. Exp. Physiol., 61: 203–254, 1976.
 32. Boyd, I. A., M. H. Gladden, P. N. McWilliam, and J. Ward. Control of dynamic and static nuclear bag fibres and nuclear chain fibres by gamma and beta axons in isolated cat muscle spindles. J. Physiol. London, 265: 133–162, 1977.
 33. Boyd, I. A., M. H. Gladden, and J. Ward. The contribution of intrafusal creep to the dynamic component of the Ia afferent discharge of isolated muscle spindles. J. Physiol. London 273: 27P–28P, 1977.
 34. Boyd, I. A., and J. Ward. Motor control of nuclear bag and nuclear chain intrafusal fibres in isolated living muscle spindles from the cat. J. Physiol. London, 244: 83–112, 1975.
 35. Brown, M. C., and R. G. Butler. Studies on the site of termination of static and dynamic fusimotor fibres within muscle spindles of the tenuissimus muscle of the cat. J. Physiol. London, 233: 553–573, 1973.
 36. Brown, M. C., and R. G. Butler. An investigation into the site of termination of static gamma fibres within muscle spindles of the cat peroneus longus muscle. J. Physiol. London, 247: 131–143, 1975.
 37. Brown, M. C., A. Crowe, and P. B. C. Matthews. Observations on the fusimotor fibres of the tibialis posterior muscle of the cat. J. Physiol. London, 177: 140–159, 1965.
 38. Brown, M. C., I. Engberg, and P. B. C. Matthews. Fusimotor stimulation and the dynamic sensitivity of the secondary ending of the muscle spindle. J. Physiol. London, 189: 545–550, 1967.
 39. Brown, M. C., I. E. Engberg, and P. B. C. Matthews. The relative sensitivity to vibration of muscle receptors of the cat. J. Physiol. London, 192: 773–800, 1967.
 40. Brown, M. C., G. M. Goodwin, and P. B. C. Matthews. After‐effects of fusimotor stimulation on the response of muscle spindle primary afferent endings. J. Physiol. London, 205: 677–694, 1969.
 41. Brown, M. C., D. G. Lawrence, and P. B. C. Matthews. Static fusimotor fibres and the position sensitivity of muscle spindle receptors. Brain Res., 14: 173–187, 1969.
 42. Brown, M. C., and P. B. C. Matthews. On the subdivision of the efferent fibres to muscle spindles into static and dynamic fusimotor fibres. In: Control and Innervation of Skeletal Muscle, edited by B. L. Andrew. Dundee: Thomson, 1966, p. 18–31.
 43. Browne, J. S. The responses of muscle spindles in sheep extraocular muscles. J. Physiol. London, 251: 483–496, 1975.
 44. Burke, D., and G. Eklund. Muscle spindle activity in man during standing. Acta Physiol. Scand., 100: 187–199, 1977.
 45. Burke, D., K.‐E. Hagbarth, and L. Löfstedt. Muscle spindle responses in man to changes in load during accurate position maintenance. J. Physiol. London, 276: 159–164, 1978.
 46. Burke, D., K.‐E. Hagbarth, and L. Löfstedt. Muscle spindle activity in man during shortening and lengthening contractions. J. Physiol. London, 277: 131–142, 1978.
 47. Burke, D., K.‐E. Hagbarth, L. Löfstedt, and B. G. Wallin. The responses of human muscle spindle endings to vibration of non‐contracting muscles. J. Physiol. London, 261: 673–693, 1976.
 48. Burke, D., K.‐E. Hagbarth, L. Löfstedt, and B. G. Wallin. The responses of human muscle spindle endings to vibration during isometric contraction. J. Physiol. London, 261: 695–711, 1976.
 49. Burke, D., K.‐E. Hagbarth, and N. F. Skuse. Voluntary activation of spindle endings in human muscles temporarily paralysed by nerve pressure. J. Physiol. London, 287: 329–336, 1979.
 50. Chen, W. J., and R. E. Poppele. Static fusimotor effect on the sensitivity of mammalian muscle spindles. Brain Res., 57: 244–247, 1973.
 51. Chen, W. J., and R. E. Poppele. Small‐signal analysis of response of mammalian muscle spindles with fusimotor stimulation and a comparison with large‐signal responses. J. Neurophysiol., 41: 15–27, 1978.
 52. Cheney, P. D., and J. B. Preston. Classification and response characteristics of muscle spindle afferents in the primate. J. Neurophysiol., 39: 1–8, 1976.
 53. Cheney, P. D., and J. B. Preston. Classification of fusimotor fibers in the primate. J. Neurophysiol., 39: 9–19, 1976.
 54. Cheney, P. D., and J. B. Preston. Effects of fusimbtor stimulation on dynamic and position sensitivities of spindle afferents in the primate. J. Neurophysiol., 39: 20–30, 1976.
 55. Cody, F. W. J., L. M. Harrison, and A. Taylor. Analysis of activity of muscle spindles of jaw‐closing muscles during normal movements in the cat. J. Physiol. London, 253: 565–582, 1975.
 56. Cody, F. W. J., R. W. H. Lee, and A. Taylor. A functional analysis of the components of the mesencephalic nucleus of the fifth nerve of the cat. J. Physiol. London, 226: 249–261, 1972.
 57. Coërs, C., and J. Durand. Données morphologiques nouvelles sur l'innervation des fuseaux neuromusculaires. Arch. Biol., 67: 685–715, 1956.
 58. Cooper, S. The responses of the primary and secondary endings of muscle spindles with intact motor innervation during applied stretch. Q. J. Exp. Physiol., 46: 389–398, 1961.
 59. Cooper, S., and P. M. Daniel. Muscle spindles in man; their morphology in the lumbricals and the deep muscles of the neck. Brain, 86: 563–586, 1963.
 60. Cooper, S., and M. H. Gladden. Elastic fibres and reticulin of mammalian muscle spindles and their functional significance. Q. J. Exp. Physiol., 59: 367–385, 1974.
 61. Critchlow, V., and C. von Euler. Intercostal muscle spindle activity and its γ‐motor control. J. Physiol. London, 168: 820–847, 1963.
 62. Crowe, A., and P. B. C. Matthews. The effects of stimulation of static and dynamic fusimotor fibres on the response to stretching of the primary endings of muscle spindles. J. Physiol. London, 174: 109–131, 1964.
 63. Crowe, A., and P. B. C. Matthews. Further studies of static and dynamic fusimotor fibres. J. Physiol. London, 174: 132–151, 1964.
 64. Cussons, P. D., M. Hulliger, and P. B. C. Matthews. Effects of fusimotor stimulation on the response of the secondary ending of the muscle spindle to sinusoidal stretching. J. Physiol. London, 270: 835–850, 1977.
 65. Durkovic, R. G., and J. B. Preston. Evidence of dynamic fusimotor excitation of secondary muscle spindle afferents in soleus muscle of cat. Brain Res., 75: 320–323, 1974.
 66. Eccles, J. C., and C. S. Sherrington. Numbers and contraction‐values of individual motor‐units examined in some muscles of the limb. Proc. R. Soc. London Ser. B, 106: 326–357, 1930.
 67. Eccles, R. M., and A. Lundberg. Integrative pattern of Ia synaptic actions on motoneurones of hip and knee muscles. J. Physiol. London, 144: 271–298, 1958.
 68. Edström, L., and E. Kugelberg. Histochemical composition, distribution of fibres and fatiguability of rat soleus motor units. J. Neurol. Neurosurg. Psychiatry, 31: 424–433, 1968.
 69. Eldred, E., R. Granit, and P. A. Merton. Supraspinal control of the muscle spindle and its significance. J. Physiol. London, 122: 498–523, 1953.
 70. Eldred, E., H. Yellin, L. Gadbois, and S. Sweeney. Bibliography on muscle receptors; their morphology, pathology and physiology. Exp. Neurol. Suppl., 3: 1–154, 1967.
 71. Eldred, E., H. Yellin, M. DeSantis, and C. M. Smith. Supplement to bibliography on muscle receptors: their morphology, pathology, physiology and pharmacology. Exp. Neurol., 55: 1–118, 1977.
 72. Ellaway, P. H., F. Emonet‐Dénand, M. Joffroy, and Y. Laporte. Lack of exclusively fusimotor α‐axons in flexor and extensor leg muscles of the cat. J. Neurophysiol., 35: 149–153, 1972.
 73. Emonet‐Dénand, F., M. Hulliger, P. B. C. Matthews, and J. Petit. Factors affecting modulation in post‐stimulus histograms on static fusimotor stimulation. Brain Res., 134: 180–184, 1977.
 74. Emonet‐Dénand, F., L. Jami, and Y. Laporte. Skeleto‐fusimotor axons in hind‐limb muscles of the cat. J. Physiol. London, 249: 153–166, 1975.
 75. Emonet‐Dénand, F., L. Jami, Y. Laporte, and N. Tankov. Glycogen depletion elicited in peroneus brevis by static α axons. Neurosci. Lett. Suppl. 1: 93, 1978.
 76. Emonet‐Dénand, F., E. Jankowsaka, and Y. Laporte. Skeleto‐fusimotor fibres in the rabbit. J. Physiol. London, 120: 669–680, 1970.
 77. Emonet‐Dénand, F., and Y. Laporte. Proportion of muscle spindles supplied by skeletofusimotor axons (β‐axons) in peroneus brevis muscle of the cat. J. Neurophysiol., 38: 1390–1394, 1975.
 78. Emonet‐Dénand, F., Y. Laporte, P. B. C. Matthews, and J. Petit. On the sub‐division of static and dynamic fusimotor actions on the primary ending of the cat muscle spindle. J. Physiol. London, 268: 827–861, 1977.
 79. Emonet‐Dénand, F., Y. Laporte, and B. Pagès. Fibres fusimotrices statiques et fibres fusimotrices dynamiques chez le lapin. Arch. Ital. Biol., 104: 195–213, 1966.
 80. Gladden, M. H. Structural features relative to the function of intrafusal muscle fibres in the cat. In: Progress in Brain Research. Understanding the Stretch Reflex, edited by S. Homma. Amsterdam: Elsevier, 1976, vol. 44, p. 51–59.
 81. Gladden, M. H., and P. N. McWilliam. The activity of intrafusal fibres during cortical stimulation in the cat. J. Physiol. London 273: 28P–29P, 1977.
 82. Goodwin, G. M., M. Hulliger, and P. B. C. Matthews. The effects of fusimotor stimulation during small amplitude stretching on the frequency‐response of the primary ending of the mammalian muscle spindle. J. Physiol. London, 253: 175–206, 1975.
 83. Goodwin, G. M., and E. S. Luschei. Effects of destroying spindle afferents from jaw muscles on mastication in monkeys. J. Neurophysiol., 37: 967–981, 1974.
 84. Goodwin, G. M., and E. S. Luschei. Discharge of spindle afferents from jaw‐closing muscles during chewing in alert monkeys. J. Neurophysiol., 38: 560–571, 1975.
 85. Goodwin, G. M., D. I. McCloskey, and P. B. C. Matthews. The contribution of muscle afferents to kinaesthesia shown by vibration induced illusions of movement and by the effects of paralysing joint afferents. Brain, 95: 705–748, 1972.
 86. Granit, R. (editor). Muscular Afferents and Motor Control. Stockholm: Almqvist and Wiksell, 1966. (Proc. Nobel Symp. I, Stockholm, 1965.)
 87. Granit, R. The Basis of Motor Control. London: Academic, 1970.
 88. Granit, R., and B. R. Kaada. Influence of stimulation of central nervous structures on muscle spindles in cat. Acta Physiol. Scand., 27: 130–160, 1952.
 89. Gregory, J. E., A. Prochazka, and U. Proske. Responses of muscle spindles to stretch after a period of fusimotor activity compared in freely moving and anaesthetized cats. Neurosci. Lett., 4: 67–72, 1977.
 90. Gregory, J. E., and U. Proske. The responses of Golgi tendon organs to stimulation of different combinations of motor units. J. Physiol. London, 295: 251–262, 1979.
 91. Harker, D. W., L. Jami, Y. Laporte, and J. Petit. Fast‐conducting skeletofusimotor axons supplying intrafusal chain fibers in the cat peroneus tertius muscle. J. Neurophysiol., 40: 791–799, 1977.
 92. Harvey, R. J., and P. B. C. Matthews. The response of de‐efferented muscle spindle endings in the cat's soleus to slow extension in the muscle. J. Physiol. London, 157: 370–392, 1961.
 93. Hasan, Z., and J. C. Houk. Analysis of response properties of deefferented mammalian spindle receptors based on frequency response. J. Neurophysiol., 38: 663–672, 1975.
 94. Hasan, Z., and J. C. Houk. Transition in sensitivity of spindle receptors that occurs when muscle is stretched more than a fraction of a millimeter. J. Neurophysiol., 38: 673–689, 1975.
 95. Hoffman, H. Local re‐innervation in partially denervated muscle: a histophysiological study. Aust. J. Exp. Biol. Med. Sci., 28: 383–392, 1950.
 96. Homma, S. (editor). Progress in Brain Research. Understanding the Stretch Reflex. Amsterdam: Elsevier, 1976, vol. 44.
 97. Houk, J. C. The phylogeny of muscular control configurations. In: Biocybernetics, edited by H. Drischel, and P. Dettmar. Jena: Fischer, 1972, vol. iv, p. 337–344.
 98. Houk, J. C., and E. Henneman. Responses of Golgi tendon organs to active contractions of the soleus muscle of the cat. J. Neurophysiol., 30: 466–481, 1967.
 99. Houk, J. C., J. J. Singer, and E. Henneman. Adequate stimulus for tendon organs with observations on mechanics of ankle joint. J. Neurophysiol., 34: 1051–1065, 1971.
 100. Hulliger, M. The responses of primary spindle afferents to fusimotor stimulation at constant and abruptly changing rates. J. Physiol. London, 294: 461–482, 1979.
 101. Hulliger, M., P. B. C. Matthews, and J. Noth. Effects of static and of dynamic fusimotor stimulation on the response of Ia fibres to low frequency sinusoidal stretching covering a wide range of amplitudes. J. Physiol. London, 267: 811–838, 1977.
 102. Hulliger, M., P. B. C. Matthews, and J. Noth. Effects of combining static and dynamic fusimotor stimulation on the response of the muscle spindle primary ending to sinusoidal stretching. J. Phyiol. London, 267: 839–856, 1977.
 103. Hunt, C. C. Relation of function to diameter in afferent fibres of muscle nerves. J. Gen. Physiol., 38: 117–131, 1954.
 104. Hunt, C. C. (editor). Handbook of Sensory Physiology. Muscle Receptors. Berlin: Springer‐Verlag, 1974, vol. 3, pt. 2.
 105. Hunt, C. C., and D. Ottoson. Impulse activity and receptor potential of primary and secondary endings of isolated mammalian muscle spindles. J. Physiol. London, 252: 259–281, 1975.
 106. Hunt, C. C., and D. Ottoson. Initial burst of primary endings of isolated mammalian muscle spindles. J. Neurophysiol., 39: 324–330, 1976.
 107. Hunt, C. C., and A. S. Paintal. Spinal reflex regulation of fusimotor neurones. J. Physiol. London, 143: 195–212, 1958.
 108. Hutton, R. S., J. L. Smith, and E. Eldred. Postcontraction sensory discharge from muscle and its source. J. Neurophysiol., 36: 1090–1103, 1973.
 109. Hutton, R. S., J. L. Smith, and E. Eldred. Persisting changes in sensory and motor activity of a muscle following its reflex activation. Pfluegers Arch., 353: 327–336, 1975.
 110. Jami, L., D. Lan‐couton, K. Malmgren, and J. Petit. “Fast” and “slow” skeletofusimotor innervation in cat tenuissimus spindles; a study with the glycogen‐depletion method. Acta Physiol. Scand., 103: 284–298, 1978.
 111. Jami, L., and J. Petit. Frequency of tendon organ discharges elicited by the contraction of motor units in cat leg muscles. J. Physiol. London, 261: 633–645, 1976.
 112. Jami, L., and J. Petit. Heterogeneity of motor units activating single Golgi endon organs in cat leg muscles. Exp. Brain Res., 24: 485–493, 1976.
 113. Jami, L., and J. Petit. Fusimotor actions on sensitivity of spindle secondary endings to slow muscle stretch in cat peroneus tertius. J. Neurophysiol., 41: 860–869, 1978.
 114. Jansen, J. K. S., and P. B. C. Matthews. The dynamic responses to slow stretch of muscle spindles in the decerebrate cat. J. Physiol. London 159: 20P–22P, 1961.
 115. Jansen, J. K. S., and P. B. C. Matthews. The central control of the dynamic response of muscle spindle receptors. J. Physiol. London, 161: 357–373, 1962.
 116. Jansen, J. K. S., and P. B. C. Matthews. The effects of fusimotor activity on the static responsiveness of primary and secondary endings of muscle spindles in the decerebrate cat. Acta Physiol. Scand., 55: 376–386, 1962.
 117. Keller, E. L., and D. A. Robinson. Absence of a stretch reflex in extraocular muscles of the monkey. J. Neurophysiol., 34: 908–919, 1971.
 118. Koeze, T. H. The response to stretch of muscle spindle afferents of baboon's tibialis anticus and the effect of fusimotor stimulation. J. Physiol. London, 197: 107–121, 1968.
 119. Koeze, T. H. Muscle spindle afferents in the baboon. J. Physiol. London, 229: 297–317, 1973.
 120. Kuffler, S. W., and C. C. Hunt. The mammalian small‐nerve fibres; a system for efferent nervous regulation of muscle spindle discharge. Res. Publ. Assoc. Res. Nerv. Ment. Dis., 30: 24–37, 1952.
 121. Kuffler, S. W., C. C. Hunt, and J. P. Quilliam. Function of medullated small‐nerve fibres in mammalian ventral roots: efferent muscle spindle innervation. J. Neurophysiol., 14: 29–54, 1951.
 122. Langley, J. N. The nerve fibre constitution of peripheral nerves and of nerve roots. J. Physiol. London, 56: 382–396, 1922.
 123. Leksell, L. The action potential and excitatory effects of the small ventral root fibres to skeletal muscle. Acta Physiol. Scand. 10: (Suppl. 31) 1–84, 1945.
 124. Lennerstrand, G. Position and velocity sensitivity of muscle spindles in the cat. I. Primary and secondary endings deprived of fusimotor activation. Acta Physiol. Scand., 73: 281–299, 1968.
 125. Lennerstrand, G. Position and velocity sensitivity of muscle spindles in the cat. IV. Interaction between two fusimotor fibres converging on the same spindle ending. Acta Physiol. Scand., 74: 257–273, 1968.
 126. Lennerstrand, G., and U. Thoden. Fusimotor effects on position and velocity sensitivity of muscle spindles. Experientia, 23: 205–206, 1967.
 127. Lennerstrand, G., and U. Thoden. Dynamic analysis of muscle spindle endings in the cat soleus using length changes of different length‐time relations. Acta Physiol. Scand., 73: 234–250, 1968.
 128. Lennerstrand, G., and U. Thoden. Position and velocity sensitivity of muscle spindles in the cat. II. Dynamic fusimotor single‐fibre activation of primary endings. Acta Physiol. Scand., 74: 16–29, 1968.
 129. Lennerstrand, G., and U. Thoden. Position and velocity sensitivity of muscle spindles in the cat. III. Static fusimotor single‐fibre activation of primary and secondary endings. Acta Physiol. Scand., 74: 30–49, 1968.
 130. Lennerstrand, G., and U. Thoden. Muscle spindle responses to concomitant variations in length and in fusimotor activation. Acta Physiol. Scand., 74: 153–165, 1968.
 131. Lewis, D. M., and U. Proske. The effect of muscle length and rate of fusimotor stimulation on the frequency of discharge in primary endings from muscle spindles in the cat. J. Physiol. London, 122: 511–535, 1972.
 132. Lundberg, A., and G. Winsbury. Selective activation of large afferents from muscle spindles and Golgi tendon organs. Acta Physiol. Scand., 49: 155–164, 1960.
 133. Matthews, B. H. C. Nerve endings in mammalian muscle. J. Physiol. London, 78: 1–53, 1933.
 134. Matthews, P. B. C. The differentiation of two types of fusimotor fibre by their effects on the dynamic response of muscle spindle primary endings. Q. J. Exp. Physiol., 47: 324–333, 1962.
 135. Matthews, P. B. C. The response of de‐efferented muscle spindle receptors to stretching at different velocities. J. Physiol. London, 168: 660–678, 1963.
 136. Matthews, P. B. C. Muscle spindles and their motor control. Physiol. Rev., 44: 219–288, 1964.
 137. Matthews, P. B. C. The origin and functional significance of the stretch reflex. In: Excitatory Synaptic Mechanisms, edited by P. Andersen, and J. K. S. Jansen. Oslo: Universitetsforlaget, 1970, p. 301–315.
 138. Matthews, P. B. C. Mammalian Muscle Receptors and their Central Actions. London: Arnold, 1972.
 139. Matthews, P. B. C., and R. B. Stein. The sensitivity of muscle spindle afferents to sinusoidal stretching. J. Physiol. London, 200: 723–743, 1969.
 140. Matthews, P. B. C., and R. B. Stein. The regularity of primary and secondary muscle spindle afferent discharges. J. Physiol. London, 202: 59–82, 1969.
 141. Matthews, P. B. C., and D. R. Westbury. Some effects of fast and slow motor fibres on muscle spindles of the frog. J. Physiol. London, 178: 178–192, 1965.
 142. McCloskey, D. I. Differences between the senses of movement and position shown by the effects of loading and vibration of muscles in man. Brain Res., 61: 119–131, 1973.
 143. McWilliam, P. N. The incidence and properties of β axons to muscle spindles in the cat hind limb. Q. J. Exp. Physiol., 60: 25–36, 1975.
 144. Merton, P. A. Speculations on the servo‐control of movement. In: The Spinal Cord, edited by G. E. W. Wolstenholme. London: Churchül, 1953, p. 247–255.
 145. Murthy, K. S. K. Vertebrate fusimotor neurones and their influences on motor behaviour. Prog. Neurobiol. Oxford, 11: 249–307, 1978.
 146. Newsom Davis, J. The response to stretch of human intercostal muscle spindles studied in vitro. J. Physiol. London, 249: 561–579, 1975.
 147. Ovalle, W. K., and R. S. Smith. Histochemical identification of three types of intrafusal muscle fibres in the cat and monkey based on the myosin ATPase reaction. Can. J. Physiol. Pharmacol., 50: 195–202, 1972.
 148. Phillips, C. G. Motor apparatus of the baboon's hand. Proc. R. Soc. London Ser. B, 173: 141–174, 1969.
 149. Poppele, R. E., and R. J. Bowman. Quantitative description of linear behavior of mammalian muscle spindles. J. Neurophysiol., 33: 59–72, 1970.
 150. Poppele, R. E., and W. J. Chen. Repetitive firing behavior of mammalian muscle spindle. J. Neurophysiol., 35: 357–364, 1972.
 151. Poppele, R. E., and W. R. Kennedy. Comparison between behaviour of human and cat muscle spindles recorded in vitro. Brain Res., 75: 316–319, 1974.
 152. Pringle, J. W. S. Stretch activation of muscle: function and mechanism. Proc. R. Soc. London Ser. B, 201: 107–130, 1978.
 153. Prochazka, A., J. A. Stephens, and P. Wand. Muscle spindle discharges in normal and obstructed movements. J. Physiol. London, 287: 57–66, 1979.
 154. Prochazka, A., R. A. Westerman, and S. P. Ziccone. Discharges of single hindlimb afferents in the freely moving cat. J. Neurophysiol., 39: 1090–1104, 1976.
 155. Prochazka, A., R. A. Westerman, and S. P. Ziccone. Ia afferent activity during a variety of voluntary movements in the cat. J. Physiol. London, 268: 423–448, 1977.
 156. Proske, U. Stretch‐evoked potentiation of responses of muscle spindles in the cat. Brain Res., 88: 378–383, 1975.
 157. Proske, U., and J. E. Gregory. The time‐course of recovery of the initial burst of primary endings of muscle spindles. Brain Res., 121: 358–361, 1977.
 158. Proske, U., and R. M. A. P. Ridge. Extrafusal muscle and muscle spindles in reptiles. Prog. Neurobiol. Oxford, 3: 3–29, 1974.
 159. Rack, P. M. H., and D. R. Westbury. The effects of suxamethonium and acetylcholine on the behaviour of cat muscle spindles during dynamic stretching, and during fusimotor stimulation. J. Physiol. London, 186: 698–713, 1966.
 160. Reinking, R. M., J. A. Stephens, and D. G. Stuart. The tendon organs of cat medial gastrocnemius: significance of motor unit type and size for the activation of Ib afferents. J. Physiol. London, 250: 491–512, 1975.
 161. Renkin, B. Z., and Å. B. Vallbo. Simultaneous responses of groups I and II cat muscle spindle afferents to muscle position and movement. J. Neurophysiol., 27: 429–450, 1964.
 162. Ruffini, A. On the minute anatomy of the neuromuscular spindles of the cat, and on their physiological significance. J. Physiol. London, 23: 190–208, 1898.
 163. Rymer, W. Z., J. C. Houk, and P. E. Crago. The relation between dynamic response and velocity sensitivity for muscle spindle receptors. Proc. Int. Union Physiol. Sci. 13: 1992, 1977.
 164. Schäfer, S. S. The acceleration response of a primary muscle‐spindle ending to a ramp stretch of the extrafusal muscle. Experientia, 23: 1026–1027, 1967.
 165. Schäfer, S. S. The characteristic curves of the dynamic response of primary muscle spindle endings in the absence and presence of stimulation of fusimotor fibres. Brain Res., 59: 395–399, 1973.
 166. Schäfer, S. S. The discharge frequencies of primary muscle spindle endings during simultaneous stimulation of two fusimotor fibres. Pfluegers Arch., 350: 359–372, 1974.
 167. Schäfer, S. S., and S. Kijewski. The dependency of the acceleration response of primary muscle spindle endings on the mechanical properties of muscle. Pfluegers Arch., 350: 101–122, 1974.
 168. Sherrington, C. S. On the anatomical constitution of nerves of skeletal muscles; with remarks on recurrent fibres in the ventral spinal nerve‐root. J. Physiol. London, 17: 211–258, 1894.
 169. Shik, M. L., G. N. Orlovskii, and F. V. Severin. Organisation of locomotor synergism. Biophysics 11: 1011–1019, 1966. (Transl. of Biofizika, 11: 879–886, 1966.)
 170. Stauffer, E. K., and J. A. Stephens. The tendon organs of cat soleus: static sensitivity to active force. Exp. Brain Res., 23: 279–291, 1975.
 171. Stauffer, E. K., and J. A. Stephens. Responses of Golgi tendon organs to ramp‐and‐hold profiles of contractile force. J. Neurophysiol., 40: 681–691, 1977.
 172. Stein, R. B. Peripheral control of movement. Physiol. Rev., 54: 215–243, 1974.
 173. Stein, R. B., and A. S. French. Models for the transmission of information by nerve cells. In: Excitatory Synaptic Mechanisms, edited by P. Andersen, and J. K. S. Jansen. Oslo: Universitetsforlaget, 1970, p. 247–257.
 174. Stephens, J. A., R. M. Reinking, and D. G. Stuart. Tendon organs of cat medial gastrocnemius: responses to active and passive forces as a function of muscle length. J. Neurophysiol., 38: 1217–1231, 1975.
 175. Stuart, D. G., G. E. Goslow, C. G. Mosher, and R. M. Reinking. Stretch responsiveness of Golgi tendon organs. Exp. Brain Res., 10: 463–476, 1970.
 176. Stuart, D. G., C. G. Mosher, R. L. Gerlac, and R. M. Reinking. Selective activation of Ia afferents by transient muscle stretch. Exp. Brain Res., 10: 477–487, 1970.
 177. Stuart, D. G., C. G. Mosher, R. L. Gerlach, and R. M. Reinking. Mechanical arrangement and transducing properties of Golgi tendon organs. Exp. Brain Res., 14: 274–292, 1972.
 178. Stuart, D. G., W. D. Willis, and R. M. Reinking. Stretch‐evoked excitatory postsynaptic potentials in motoneurons. Brain Res., 33: 115–125, 1971.
 179. Swash, M., and K. P. Fox. Muscle spindle innervation in man. J. Anat., 112: 61–80, 1972.
 180. Vallbo, Å. B. Slowly adapting muscle receptors in man. Acta Physiol. Scand., 78: 315–333, 1970.
 181. Vallbo, Å. B. Discharge patterns in human muscle spindle afferents during isometric voluntary contractions. Acta Physiol. Scand., 80: 552–566, 1970.
 182. Vallbo, Å. B. Afferent discharge from human muscle spindles in noncontracting muscles. Steady state impulse frequency as a function of joint angle. Acta Physiol. Scand., 90: 303–318, 1974.
 183. Vallbo, Å. B. Human muscle spindle discharge during isometric voluntary contractions. Amplitude relations between spindle frequency and torque. Acta Physiol. Scand., 90: 319–336, 1974.
 184. Vallbo, Å. B., K.‐E. Hagbarth, H. E. Torebjork, and B. G. Wallin. Somatosensory, proprioceptive, and sympathetic activity in human peripheral nerves. Physiol. Rev., 59: 919–957, 1979.
 185. Windhorst, U., J. Meyer‐Lohmann, and J. Schmidt. Correlation of the dynamic behaviour of deefferented primary muscle endings with their static behaviour. Pfluegers Arch., 357: 113–122, 1975.
 186. Yellin, H. A histochemical study of muscle spindles and their relationship to extrafusal fibre types in the rat. Am. J. Anat., 125: 31–37, 1969.

Contact Editor

Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite

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