Reflexes Evoked by Group II Afferent Fibers from Muscle Spindles NANCY L. URBSCHEIT, PhD
Key Words: Neurophysiology, Reflex.
Physical therapists have commonly been taught that excitation of group II afferent fibers arising from the secondary sensory endings of muscle spindles will facilitate flexor muscles and inhibit extensor muscles. This basic concept has been incorporated into pro cedures of therapeutic exercise. For example, an ap proach developed by Rood and interpreted by Stockmeyer suggests that activation of II afferent fibers from muscle spindles can achieve cocontraction of antagonistic muscles. 1 Supposedly, if a group of ex tensor muscles contract volitionally while resistance is applied, the group II afferent fibers from these muscles will increase their discharge. This activation of group II afferent fibers is assumed to promote reflexly contraction of the antagonistic flexor muscles, resulting in a cocontraction of the muscle groups about the joint. Such descriptions of the reflex actions of the group II afferent fibers from muscle spindles are simplistic and subject to criticism because of much experimental evidence that these afferent fibers can evoke several different reflexes under various condi tions. In order to describe appropriately and use the reflexes produced by activation of the group II affer-
Dr. Urbscheit was Assistant Professor, Graduate Program in Physical Therapy. University of Iowa, Iowa City, IA 52242, when this paper was written. She now resides at 3508 Brisbane, Lansing. MI 48910. This article was submitted February 2, 1978, and accepted April 20, 1979.
Volume 59 / Number 9, September 1979
ent fibers of the muscle spindles, physical therapists must understand the scientific literature on the action of these fibers. The purpose of this paper is to review the literature on the reflex action of the secondary sensory endings and to offer an analysis of its signif icance to physical therapy. THE CLASSICAL CONCEPT
The classical reflex pathway and action of the group II afferent fibers from the muscle spindle is diagrammed in Figure 1. The conclusion that group II afferent fibers facilitate flexor muscles and inhibit extensor muscles was generated from experiments on cats with complete spinal cord transections at the lumbar level. 2 ' In these animals, electrical activity of alpha motoneurons below the level of the lesion was recorded by intracellular electrodes. In order to ob serve the action of the group II afferent fibers on these alpha motoneurons, the fibers were electrically stimulated through the peripheral nerves. The exper iments revealed that stimulation of the group II af ferent fibers facilitated (depolarized) alpha motoneu rons innervating flexor muscles and inhibited (hyperpolarized) alpha motoneurons innervating extensor muscles. These effects were assumed to be mediated by polysynaptic pathways because of the relatively long latency between the electrical stimulation of the group II afferent fibers and the response from the alpha motoneurons. 1083
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The purpose of this paper is to review research on the reflex action of group II afferent fibers originating in the muscle spindle. Although the reflex actions of the la afferent fibers from muscle spindles are well defined, the reflex action of the group II afferent fibers is not clearly understood. Experiments on animals whose spinal cord had been transected gave rise to the idea that group II afferent fibers facilitate flexor muscles and inhibit extensor muscles regardless of the origin of the fibers. This concept has been accepted by neurophysiologists and has even been incorporated into therapeutic exercise procedures by physi cal therapists. However, accumulating evidence is presented that challenges this classical concept. Physical therapists, when trying to incorporate the re flexes evoked by the group II afferent fibers into treatment, must become better aware of the complex reflex actions of which these fibers are capable.
Extensor
rr? Fig. 1. Schematic illustration of classical reflex action of group II afferent fibers from muscle spindles (a = alpha motoneuron, II = group II afferent fiber, + = facilitation, — = inhibition).
A CRITIQUE OF THE CLASSICAL CONCEPT The reflex action evoked from group II afferent fibers of muscle spindles, however, is not as simple as these earlier experiments might suggest. For example, the reflex action of the group II afferent fibers changes if the condition of the experimental animal is altered. In the early experiments just described, several of the spinal cats developed very low blood pressure. :i In these animals, stimulation of the group II afferent fibers in the peripheral nerves produced the opposite effect, that is, facilitation of extensor alpha motoneu rons and inhibition of the flexor alpha motoneurons. In addition, Wilson and Kato recorded electrical activity of alpha motoneurons innervating hind-limb muscles in cats whose spinal cords had been tran sected at the atlantooccipital region. 4 In these cats with transections at high levels of the spinal cord, electrical stimulation of group II afferent fibers in peripheral nerves frequently produced excitation, rather than inhibition, of extensor alpha motoneu rons. Not all experiments on the reflex action of group II afferent fibers have been done on spinal animals. Kuno and Perl studied reflexes evoked from group II afferent fibers in spastic decerebrate cats.' Electrical stimulation of group II afferent fibers in these cats produced no change in the excitability of either flexor or extensor alpha motoneurons. Yet, upon subsequent 1084
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Flexor
spinal cord transection, stimulation of group II fibers did result in the classical facilitation of flexor alpha motoneurons and inhibition of extensor alpha moto neurons. Matthews also attempted to assess the reflex action of the group II afferent fibers in the spastic decere brate cat/' He studied the amplitude of the contractile response of the spastic triceps surae muscle to main tained stretch and to vibration of the Achilles tendon. When the spastic triceps surae muscle was held in a maintained stretch, the muscle responded with a maintained contraction. This reflex, the tonic stretch reflex, had been assumed to be evoked by the exci tation of the primary sensory endings of the muscle spindles.' Vibration of a muscle is known to excite preferentially the primary sensory endings of muscle spindles and, like maintained stretch, can also evoke a tonic contraction from the muscle (tonic vibration reflex).* 1 ' Thus, the tonic stretch reflex and the tonic vibration reflex appear to involve the same sensory receptor and afferent pathway. If both the tonic stretch reflex and the tonic vibra tion reflex depend upon the same receptor and path way, there should be no summation of muscle tension resulting from the simultaneous application of vibra tion and tonic stretch. Yet, when the spastic triceps surae muscle of the decerebrate cat was both stretched and vibrated, the muscle developed additional ten sion. The explanation offered by Matthews for this surprising result is that the contractile response to stretch is largely due to the activation of secondary sensory endings of the spindle. Therefore, the reflex response to vibration had not been occluded by the stretch, because many of the primary sensory endings were still capable of responding to the imposed vibra tion. Matthews also wished to compare the relative strengths of the tonic vibration reflex and the tonic stretch reflex. He observed that vibration of the Achilles tendon of the spastic triceps surae muscle at an amplitude of 150 ju produced 3.9 gm of tension per hertz of vibration. A maintained stretch of the spastic triceps surae muscle produced 90 gm of tension per millimeter of stretch. Presuming that vibration was driving all the primary sensory endings and that each la afferent fiber was discharging at the frequency of vibration, Matthews calculated the frequency of lafiber discharge to be 23 Hz/mm stretch (90 gm/mm divided by 3.9 Hz/gm). However, other investigators who have actually recorded discharge from la afferent fibers originating in the triceps surae muscle of de cerebrate cats have found that the la fibers actually discharge at only 2-5 Hz per millimeter of stretch. 10 Thus, the tension produced by maintained stretch appears to be too great to be solely evoked by la PHYSICAL THERAPY
Volume 59 / Number 9, September 1979
ments the reflex response to simultaneous vibration and stretch was examined in decerebrate cats before and after fusimotor paralysis by procaine. Procaine blocks the response of the sensory endings of the muscle spindle to maintained stretch, thus abolishing the tonic stretch reflex but not the tonic vibration reflex. On this basis, Matthews predicted that the reflex tension developed during the application of simultaneous stretch and vibration would not be af fected by procaine block if la afferent fibers are solely responsible for the tonic stretch reflex. However, the fusimotor block did reduce the tension evoked by combined vibration and stretch. This reduction was attributed to the loss of excitatory input from fibers other than the la afferent fibers. The II afferent fibers from the spindle were implicated because their firing is known to be decreased by fusimotor block. Experiments by other investigators have also sup ported the concept of excitation of extensor alpha motoneurons from group II afferent fiber input. Westbury made intracellular recordings of the electrical activity of alpha motoneurons innervating the spastic triceps surae muscle in decerebrate cats during vibra tion and stretch of that muscle.17 The amplitude of depolarization evoked by maintained stretch was gen erally greater than that evoked by vibration. In ad dition, there was no occlusion during simultaneous stretch and vibration. Such observations again suggest that the tonic vibration reflex and the tonic stretch reflex depend upon different afferent pathways. There is also evidence that group II afferent fibers can exert an indirect excitatory action (disinhibition) on extensor alpha motoneurons, as Matthews sug gested. For example, Fromm and associates found that group II afferent fibers in the nerve of the gastrocnemius muscle in decerebrate cats can reduce recurrent inhibition of the gastrocnemius alpha mo toneurons, rendering the gastrocnemius motoneurons more excitable.18 Kirkwood and Sears reported a rather startling action of group II afferent fibers that may partially explain Matthews' results. These investigators re corded electrical discharge from alpha motoneurons innervating internal intercostal muscles of anesthe tized, but neurologically normal, cats.19 The internal intercostal muscles were stretched and the discharge of spindle afferent fibers was recorded from nerve filaments supplying the muscle. An impulse in an afferent fiber was used to trigger a signal averager so that the recordings of reflex synaptic potentials evoked from the intercostal motoneurons could be extracted from ordinary synaptic noise. The compos ite synaptic potentials evoked from a motoneuron by stretch could then be divided into unitary potentials based on latency, rise time, and amplitude. The group 1085
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afferent-fiber discharge. From these observations, Matthews suggests that the secondary sensory endings of the muscle spindle, which are excited by stretch but not by vibration, are responsible for the discrep ancy. Matthews further suggests that discharge of the spindle group II afferent fibers may even be respon sible for the spasticity of the triceps surae muscle in these decerebrate cats. Matthews' conclusions are controversial; criticisms as well as other explanations have been offered for his observations. Grillner chal lenged Matthews' interpretation that the tension evoked during a tonic stretch reflex is too great to be accounted for solely by la afferent-fiber discharge.11 Grillner suggested that the tension developed by a muscle during maintained stretch depends upon its length-tension relationship as well as its reflex behav ior. For example, if a deafferentated muscle is made to contract isometrically by electrical stimulation of the appropriate ventral root filaments, the muscle's tension will be greater the longer the muscle's initial length.12 Cook and Duncan also challenged the concept that the group II afferent fibers are responsible for the tonic stretch reflex of spastic muscles in decerebrate cats.13 In their study, they disrupted the tonic stretch reflex of the triceps surae muscle in decerebrate cats by pressure block of the la afferent fibers. During this block the tonic stretch reflex was markedly reduced, suggesting that the la afferent fibers, rather than the group II afferent fibers, are primarily responsible for the tonic stretch reflex. Matthews' concept of the reflex action of the group II afferent fibers in the decerebrate cat, however, has not been cast aside. Matthews has addressed the criticisms in several subsequent papers.14'15 He reiter ates that his initial experiments were performed with the triceps surae muscle within the last 7 mm of the muscle's maximal length. At this length, the degree to which muscle strength varies with length decreases. In addition, Matthews states that the elimination of the tonic stretch reflex by blocking la afferent fibers can not disprove the involvement of group II afferent fibers; the group II afferent fibers may exert an indirect excitatory action on extensor motoneurons. For example, group II afferents may interfere with lb autogenic inhibition, Renshaw inhibition, or presyn aptic inhibition or may result in a facilitation of la polysynaptic pathways. Thus, group II afferents may not be capable of initiating the tonic stretch reflex in spastic muscles, but may affect the amplitude of the reflex when it is evoked. In additional experiments, McGrath and Matthews offered supportive evidence that the group II afferent fibers provide an excitatory contribution to the tonic stretch reflex of spastic muscles.16 In these experi
Lesion
Flexor
Lesion
Extensor
Extensor
Fig. 2. Schematic illustration of how the reflex action of group II afferent fibers might be affected by a brain lesion. A. Loss of supraspinal facilitation of interneurons mediating the reflex action of group II afferent fibers could reduce or abolish reflexes evoked by II afferent fibers in the normal state. B. Loss of inhibition of specific interneurons can "release" a reflex path that might not normally be activated by group II afferent fibers. For example, Renshaw cells might be inhibited by group II afferent fibers following brain damage. This change in turn would result in an indirect facilitation of extensor alpha motoneurons (a = alpha motoneuron, II = group II afferent fiber, + = facilitation, — = inhibition, R = Renshaw cell).
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"switched on or off' after brain lesions, thus changing the reflex action of the group II afferent fibers (Fig. 2). At present, it is not clear if brain lesions alter the excitatory monosynaptic action of group II afferent fibers on alpha motoneurons. STUDIES IN MAN Not all experimentation on the reflex action of group II afferent fibers has been done on lower animals. Burke and associates21'22 studied the stretch reflexes of the quadriceps femoris and hamstring muscles in spastic patients with spinal cord lesions. They examined the amplitude of the EMG of each muscle in response to an abrupt, short stretch when the knee was in different positions. As the knee was placed in positions of greater initial flexion, the response of the quadriceps femoris muscle to quick stretch was reduced. In contrast, as the knee was placed in positions of greater initial extension, the phasic stretch reflex of the hamstrings increased. The differential effects of muscle length on the stretch reflexes of these two muscles has been explained by the classical concept of action of the group II spindle afferent fibers. When the quadriceps femoris muscle is lengthened by knee flexion, dis charge of the group II spindle afferents from the muscle is probably increased. According to the clas sical view, this should inhibit the alpha motoneurons of the quadriceps femoris muscle. Thus, the ability of the quadriceps femoris muscle to respond to a brief stretch will be reduced when its length is increased. In contrast, the discharge of group II afferent fibers from hamstrings will be increased when the length of the muscle is progressively increased by knee exten sion. Because the hamstrings are flexor muscles, the group II afferent fibers will facilitate the hamstring alpha motoneurons and increase their responsiveness to quick stretch. Thus, the action of the II afferent fibers in spinal man resembles that of the spinal cat. The traditional concept meets with difficulty, how ever, in studies involving subjects with lesions of the brain. In subjects with athetosis and parkinsonism, a passive increase in length of the quadriceps femoris and hamstring muscles has been found to enhance the response of both muscles to phasic stretch.23'24 In similar studies involving muscles of the upper extremity, the phasic stretch reflex of the triceps brachii muscle is enhanced by length in normal, hemiplegic, athetoid, and parkinsonian subjects.20,22,23 However, the phasic stretch reflex of the biceps bra chii muscle is facilitated by length in parkinsonian and hemiplegic subjects, yet is inhibited by length in normal and athetoid subjects.23'25'26 The reasons for these differences between various patients are not
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II afferent-fiber discharge appeared to produce a monosynaptic excitation of the internal intercostal alpha motoneurons. Subsequent investigations, using similar techniques, have also revealed a monosynaptic excitation of alpha motoneurons of the triceps surae muscle by group II afferent fibers from that muscle.20 These are remarkable observations, because up to this time the only monosynaptic spinal reflex thought to exist was that evoked by the la afferent fibers from the muscle spindle. As should be obvious from the above experiments, it is not appropriate to describe the reflex action of the group II afferent fibers of the muscle spindle as being only excitatory to flexor muscles and inhibitory to extensor muscles. Rather, several different reflex actions have been found to be possible, depending in part on the animal preparation. One explanation for the diverse reflex actions is that the predominant reflex action of these group II afferent fibers is me diated by interneurons in the spinal cord. The activity of spinal interneurons is greatly influenced by su praspinal input in the normal nervous system. If supraspinal centers are damaged, the activity of spinal interneurons can be dramatically altered. Interneu rons mediating reflexes of group II afferents can be
PHYSICAL THERAPY
clear; alterations in the reflex actions of the group II afferent fibers may be involved.
1. Stockmeyer SA: An interpretation of the approach of Rood to the treatment of neuromuscular dysfunction. Proceedings: An exploratory and analytical survey of therapeutic exercise, Northwestern University. Am J Phys Med 46:900-961,1967 2. Lloyd DPC: Integrative pattern of excitation and inhibition in two-neuron reflex. J Neurophysiol 9:439-444, 1946 3. Eccles RM, Lundberg A: Synaptic actions in motoneurons by afferents which may evoke the flexion reflex. Arch Ital Biol 97:199-221, 1959 4. Wilson VJ, Kato M: Excitation of extensor motoneurons by group II afferent fibers in ipsilateral muscle nerves. J Neu rophysiol 28:545-554, 1965 5. Kuno M, Perl ER: Alteration of spinal reflexes by interaction with suprasegmental and dorsal root activity. J Physiol 151: 103-122, 1960 6. Matthews PBC: Evidence that the secondary as well as the primary endings of the muscle spindles may be responsible for the tonic stretch reflex of the decerebrate cat. J Physiol (Lond) 204:365-393, 1969 7. Matthews PBC: Mammalian Muscle Receptors and Their Central Actions. London, Edward Arnold Ltd, 1972, pp 421423 8. Bianconi R, Vander Meulen JF: The response to vibration of the end-organs of mammalian muscle spindles. J Neuro physiol 26:177-190, 1963 9. Brown MC, Engbert I, Matthews PBC: The relative sensitivity to vibration of muscle receptors of the cat. J Physiol 192: 773-800, 1967 10. Granit R: Neuromuscular interaction in postural tone of the cat's isometric soleus muscle. J Physiol 143:387-402,1958 11. Grillner S: Is the tonic stretch reflex dependent upon group II excitation? Acta Physiol Scand 38:431-432, 1970 12. Rack PMH, Westbury DR: The effects of length and stimulus rate on tension in the isometric cat soleus muscle. J Physiol 204:443-460, 1969 13. Cook WA, Duncan CC: Contribution of group I afferents to the tonic stretch reflex of the decerebrate cat. Brain Res 33: 509-513, 1971 14. Matthews PBC: A reply to criticism of the hypothesis that the group II afferents contribute excitation to the stretch reflex. Acta Physiol Scand 79:431-433, 1970
15. Matthews PBC: A critique of the hypothesis that spindle secondary endings contribute excitation to the stretch reflex. In Stein RB, Pearson KG, Smith RS, et al: Control of Posture and Locomotion. New York, Plenum Press, 1973, pp 227243 16. McGrath GJ, Matthews PBC: Evidence from the use of vibra tion during procaine nerve block that the spindle group II fibres contribute excitation to the tonic stretch reflex of the decerebrate cat. J Physiol 235:371-408, 1973 17. Westbury DR: A study of stretch and vibration reflexes of the cat by intracellular recording from motoneurones. J Physiol 226:37-56, 1972 18. Fromm C, Haase J, Wolf E: Depression of the recurrent inhibition of extensor motoneurons by the action of group II afferents. Brain Res 120:459-468, 1977 19. Kirkwood PA, Sears TA: Monosynaptic excitation of moto neurones from secondary endings of muscle spindles. Nature 252:243-244,1974 20. Kirkwood PA, Sears TA: Monosynaptic excitation of moto neurones from muscle spindle secondary endings of inter costal and triceps surae muscles in the cat. J Physiol 245: 64-65P,1975 21. Burke P, Gillies JD, Lance JW: The quadriceps stretch reflex in human spasticity. J Neurol Neurosurg Psychiatry 33:216223, 1970 22. Burke P, Gillies JD, Lance JW: Hamstrings stretch reflex in human spasticity. J Neurol Neurosurg Psychiatry 34:321325, 1971 23. Andrews CJ, Neilson P, Knowles L: Electromyographic study of the rigidospasticity of athetosis. J Neurol Neurosurg Psy chiatry 36:94-103, 1973 24. Andrews CJ, Burke D, Lance JW: The response to muscle stretch and shortening in parkinsonian rigidity. Brain 95: 795-812, 1972 25. Ashby P, Burke D: Stretch reflexes in the upper limb of spastic man. J Neurol Neurosurg Psychiatry 34:765-771, 1971 26. Andrews CJ, Neilson PD, Lance JW: Comparison of stretch reflexes and shortening reactions in activated normal sub jects with those in Parkinson's disease. J Neurol Neurosurg Psychiatry 36:329-333, 1973
CLINICAL IMPLICATIONS
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A basic message of this review is that the group II afferent fibers of the muscle spindles can exert diverse reflex actions, depending upon the integrity and state of the CNS. Thus, the reflex action of these fibers may vary widely in the neurologically involved pa tient. Therapists have attempted to use the classical reflex of flexor facilitation and extensor inhibition attributed to these afferent fibers, yet these actions may be manifested primarily in patients with spinal cord injury and may not even exist in the majority of
patients with brain damage. At the present, more experimental work needs to be done to define clearly the reflex action of the group II afferent fibers from the muscle spindle in patients with a neurological deficit. Physical therapists should be aware that pa tients with a particular brain deficit may have one type of reflex from activation of the group II afferent fibers from muscle spindles while patients with an other brain lesion may have a different response. At this time, specific brain lesions cannot be definitely associated with specific reflex actions of the group II afferent fibers. Therefore, therapists should be cau tious in making and accepting statements about the reflex action of these fibers in patients with brain damage until experimental evidence has been thor oughly developed.
Key Words: Neurophysiology, Reflex.
Physical therapists have commonly been taught that excitation of group II afferent fibers arising from the secondary sensory endings of muscle spindles will facilitate flexor muscles and inhibit extensor muscles. This basic concept has been incorporated into pro cedures of therapeutic exercise. For example, an ap proach developed by Rood and interpreted by Stockmeyer suggests that activation of II afferent fibers from muscle spindles can achieve cocontraction of antagonistic muscles. 1 Supposedly, if a group of ex tensor muscles contract volitionally while resistance is applied, the group II afferent fibers from these muscles will increase their discharge. This activation of group II afferent fibers is assumed to promote reflexly contraction of the antagonistic flexor muscles, resulting in a cocontraction of the muscle groups about the joint. Such descriptions of the reflex actions of the group II afferent fibers from muscle spindles are simplistic and subject to criticism because of much experimental evidence that these afferent fibers can evoke several different reflexes under various condi tions. In order to describe appropriately and use the reflexes produced by activation of the group II affer-
Dr. Urbscheit was Assistant Professor, Graduate Program in Physical Therapy. University of Iowa, Iowa City, IA 52242, when this paper was written. She now resides at 3508 Brisbane, Lansing. MI 48910. This article was submitted February 2, 1978, and accepted April 20, 1979.
Volume 59 / Number 9, September 1979
ent fibers of the muscle spindles, physical therapists must understand the scientific literature on the action of these fibers. The purpose of this paper is to review the literature on the reflex action of the secondary sensory endings and to offer an analysis of its signif icance to physical therapy. THE CLASSICAL CONCEPT
The classical reflex pathway and action of the group II afferent fibers from the muscle spindle is diagrammed in Figure 1. The conclusion that group II afferent fibers facilitate flexor muscles and inhibit extensor muscles was generated from experiments on cats with complete spinal cord transections at the lumbar level. 2 ' In these animals, electrical activity of alpha motoneurons below the level of the lesion was recorded by intracellular electrodes. In order to ob serve the action of the group II afferent fibers on these alpha motoneurons, the fibers were electrically stimulated through the peripheral nerves. The exper iments revealed that stimulation of the group II af ferent fibers facilitated (depolarized) alpha motoneu rons innervating flexor muscles and inhibited (hyperpolarized) alpha motoneurons innervating extensor muscles. These effects were assumed to be mediated by polysynaptic pathways because of the relatively long latency between the electrical stimulation of the group II afferent fibers and the response from the alpha motoneurons. 1083
Downloaded from https://academic.oup.com/ptj/article-abstract/59/9/1083/4560021 by guest on 20 November 2018
The purpose of this paper is to review research on the reflex action of group II afferent fibers originating in the muscle spindle. Although the reflex actions of the la afferent fibers from muscle spindles are well defined, the reflex action of the group II afferent fibers is not clearly understood. Experiments on animals whose spinal cord had been transected gave rise to the idea that group II afferent fibers facilitate flexor muscles and inhibit extensor muscles regardless of the origin of the fibers. This concept has been accepted by neurophysiologists and has even been incorporated into therapeutic exercise procedures by physi cal therapists. However, accumulating evidence is presented that challenges this classical concept. Physical therapists, when trying to incorporate the re flexes evoked by the group II afferent fibers into treatment, must become better aware of the complex reflex actions of which these fibers are capable.
Extensor
rr? Fig. 1. Schematic illustration of classical reflex action of group II afferent fibers from muscle spindles (a = alpha motoneuron, II = group II afferent fiber, + = facilitation, — = inhibition).
A CRITIQUE OF THE CLASSICAL CONCEPT The reflex action evoked from group II afferent fibers of muscle spindles, however, is not as simple as these earlier experiments might suggest. For example, the reflex action of the group II afferent fibers changes if the condition of the experimental animal is altered. In the early experiments just described, several of the spinal cats developed very low blood pressure. :i In these animals, stimulation of the group II afferent fibers in the peripheral nerves produced the opposite effect, that is, facilitation of extensor alpha motoneu rons and inhibition of the flexor alpha motoneurons. In addition, Wilson and Kato recorded electrical activity of alpha motoneurons innervating hind-limb muscles in cats whose spinal cords had been tran sected at the atlantooccipital region. 4 In these cats with transections at high levels of the spinal cord, electrical stimulation of group II afferent fibers in peripheral nerves frequently produced excitation, rather than inhibition, of extensor alpha motoneu rons. Not all experiments on the reflex action of group II afferent fibers have been done on spinal animals. Kuno and Perl studied reflexes evoked from group II afferent fibers in spastic decerebrate cats.' Electrical stimulation of group II afferent fibers in these cats produced no change in the excitability of either flexor or extensor alpha motoneurons. Yet, upon subsequent 1084
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Flexor
spinal cord transection, stimulation of group II fibers did result in the classical facilitation of flexor alpha motoneurons and inhibition of extensor alpha moto neurons. Matthews also attempted to assess the reflex action of the group II afferent fibers in the spastic decere brate cat/' He studied the amplitude of the contractile response of the spastic triceps surae muscle to main tained stretch and to vibration of the Achilles tendon. When the spastic triceps surae muscle was held in a maintained stretch, the muscle responded with a maintained contraction. This reflex, the tonic stretch reflex, had been assumed to be evoked by the exci tation of the primary sensory endings of the muscle spindles.' Vibration of a muscle is known to excite preferentially the primary sensory endings of muscle spindles and, like maintained stretch, can also evoke a tonic contraction from the muscle (tonic vibration reflex).* 1 ' Thus, the tonic stretch reflex and the tonic vibration reflex appear to involve the same sensory receptor and afferent pathway. If both the tonic stretch reflex and the tonic vibra tion reflex depend upon the same receptor and path way, there should be no summation of muscle tension resulting from the simultaneous application of vibra tion and tonic stretch. Yet, when the spastic triceps surae muscle of the decerebrate cat was both stretched and vibrated, the muscle developed additional ten sion. The explanation offered by Matthews for this surprising result is that the contractile response to stretch is largely due to the activation of secondary sensory endings of the spindle. Therefore, the reflex response to vibration had not been occluded by the stretch, because many of the primary sensory endings were still capable of responding to the imposed vibra tion. Matthews also wished to compare the relative strengths of the tonic vibration reflex and the tonic stretch reflex. He observed that vibration of the Achilles tendon of the spastic triceps surae muscle at an amplitude of 150 ju produced 3.9 gm of tension per hertz of vibration. A maintained stretch of the spastic triceps surae muscle produced 90 gm of tension per millimeter of stretch. Presuming that vibration was driving all the primary sensory endings and that each la afferent fiber was discharging at the frequency of vibration, Matthews calculated the frequency of lafiber discharge to be 23 Hz/mm stretch (90 gm/mm divided by 3.9 Hz/gm). However, other investigators who have actually recorded discharge from la afferent fibers originating in the triceps surae muscle of de cerebrate cats have found that the la fibers actually discharge at only 2-5 Hz per millimeter of stretch. 10 Thus, the tension produced by maintained stretch appears to be too great to be solely evoked by la PHYSICAL THERAPY
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ments the reflex response to simultaneous vibration and stretch was examined in decerebrate cats before and after fusimotor paralysis by procaine. Procaine blocks the response of the sensory endings of the muscle spindle to maintained stretch, thus abolishing the tonic stretch reflex but not the tonic vibration reflex. On this basis, Matthews predicted that the reflex tension developed during the application of simultaneous stretch and vibration would not be af fected by procaine block if la afferent fibers are solely responsible for the tonic stretch reflex. However, the fusimotor block did reduce the tension evoked by combined vibration and stretch. This reduction was attributed to the loss of excitatory input from fibers other than the la afferent fibers. The II afferent fibers from the spindle were implicated because their firing is known to be decreased by fusimotor block. Experiments by other investigators have also sup ported the concept of excitation of extensor alpha motoneurons from group II afferent fiber input. Westbury made intracellular recordings of the electrical activity of alpha motoneurons innervating the spastic triceps surae muscle in decerebrate cats during vibra tion and stretch of that muscle.17 The amplitude of depolarization evoked by maintained stretch was gen erally greater than that evoked by vibration. In ad dition, there was no occlusion during simultaneous stretch and vibration. Such observations again suggest that the tonic vibration reflex and the tonic stretch reflex depend upon different afferent pathways. There is also evidence that group II afferent fibers can exert an indirect excitatory action (disinhibition) on extensor alpha motoneurons, as Matthews sug gested. For example, Fromm and associates found that group II afferent fibers in the nerve of the gastrocnemius muscle in decerebrate cats can reduce recurrent inhibition of the gastrocnemius alpha mo toneurons, rendering the gastrocnemius motoneurons more excitable.18 Kirkwood and Sears reported a rather startling action of group II afferent fibers that may partially explain Matthews' results. These investigators re corded electrical discharge from alpha motoneurons innervating internal intercostal muscles of anesthe tized, but neurologically normal, cats.19 The internal intercostal muscles were stretched and the discharge of spindle afferent fibers was recorded from nerve filaments supplying the muscle. An impulse in an afferent fiber was used to trigger a signal averager so that the recordings of reflex synaptic potentials evoked from the intercostal motoneurons could be extracted from ordinary synaptic noise. The compos ite synaptic potentials evoked from a motoneuron by stretch could then be divided into unitary potentials based on latency, rise time, and amplitude. The group 1085
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afferent-fiber discharge. From these observations, Matthews suggests that the secondary sensory endings of the muscle spindle, which are excited by stretch but not by vibration, are responsible for the discrep ancy. Matthews further suggests that discharge of the spindle group II afferent fibers may even be respon sible for the spasticity of the triceps surae muscle in these decerebrate cats. Matthews' conclusions are controversial; criticisms as well as other explanations have been offered for his observations. Grillner chal lenged Matthews' interpretation that the tension evoked during a tonic stretch reflex is too great to be accounted for solely by la afferent-fiber discharge.11 Grillner suggested that the tension developed by a muscle during maintained stretch depends upon its length-tension relationship as well as its reflex behav ior. For example, if a deafferentated muscle is made to contract isometrically by electrical stimulation of the appropriate ventral root filaments, the muscle's tension will be greater the longer the muscle's initial length.12 Cook and Duncan also challenged the concept that the group II afferent fibers are responsible for the tonic stretch reflex of spastic muscles in decerebrate cats.13 In their study, they disrupted the tonic stretch reflex of the triceps surae muscle in decerebrate cats by pressure block of the la afferent fibers. During this block the tonic stretch reflex was markedly reduced, suggesting that the la afferent fibers, rather than the group II afferent fibers, are primarily responsible for the tonic stretch reflex. Matthews' concept of the reflex action of the group II afferent fibers in the decerebrate cat, however, has not been cast aside. Matthews has addressed the criticisms in several subsequent papers.14'15 He reiter ates that his initial experiments were performed with the triceps surae muscle within the last 7 mm of the muscle's maximal length. At this length, the degree to which muscle strength varies with length decreases. In addition, Matthews states that the elimination of the tonic stretch reflex by blocking la afferent fibers can not disprove the involvement of group II afferent fibers; the group II afferent fibers may exert an indirect excitatory action on extensor motoneurons. For example, group II afferents may interfere with lb autogenic inhibition, Renshaw inhibition, or presyn aptic inhibition or may result in a facilitation of la polysynaptic pathways. Thus, group II afferents may not be capable of initiating the tonic stretch reflex in spastic muscles, but may affect the amplitude of the reflex when it is evoked. In additional experiments, McGrath and Matthews offered supportive evidence that the group II afferent fibers provide an excitatory contribution to the tonic stretch reflex of spastic muscles.16 In these experi
Lesion
Flexor
Lesion
Extensor
Extensor
Fig. 2. Schematic illustration of how the reflex action of group II afferent fibers might be affected by a brain lesion. A. Loss of supraspinal facilitation of interneurons mediating the reflex action of group II afferent fibers could reduce or abolish reflexes evoked by II afferent fibers in the normal state. B. Loss of inhibition of specific interneurons can "release" a reflex path that might not normally be activated by group II afferent fibers. For example, Renshaw cells might be inhibited by group II afferent fibers following brain damage. This change in turn would result in an indirect facilitation of extensor alpha motoneurons (a = alpha motoneuron, II = group II afferent fiber, + = facilitation, — = inhibition, R = Renshaw cell).
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"switched on or off' after brain lesions, thus changing the reflex action of the group II afferent fibers (Fig. 2). At present, it is not clear if brain lesions alter the excitatory monosynaptic action of group II afferent fibers on alpha motoneurons. STUDIES IN MAN Not all experimentation on the reflex action of group II afferent fibers has been done on lower animals. Burke and associates21'22 studied the stretch reflexes of the quadriceps femoris and hamstring muscles in spastic patients with spinal cord lesions. They examined the amplitude of the EMG of each muscle in response to an abrupt, short stretch when the knee was in different positions. As the knee was placed in positions of greater initial flexion, the response of the quadriceps femoris muscle to quick stretch was reduced. In contrast, as the knee was placed in positions of greater initial extension, the phasic stretch reflex of the hamstrings increased. The differential effects of muscle length on the stretch reflexes of these two muscles has been explained by the classical concept of action of the group II spindle afferent fibers. When the quadriceps femoris muscle is lengthened by knee flexion, dis charge of the group II spindle afferents from the muscle is probably increased. According to the clas sical view, this should inhibit the alpha motoneurons of the quadriceps femoris muscle. Thus, the ability of the quadriceps femoris muscle to respond to a brief stretch will be reduced when its length is increased. In contrast, the discharge of group II afferent fibers from hamstrings will be increased when the length of the muscle is progressively increased by knee exten sion. Because the hamstrings are flexor muscles, the group II afferent fibers will facilitate the hamstring alpha motoneurons and increase their responsiveness to quick stretch. Thus, the action of the II afferent fibers in spinal man resembles that of the spinal cat. The traditional concept meets with difficulty, how ever, in studies involving subjects with lesions of the brain. In subjects with athetosis and parkinsonism, a passive increase in length of the quadriceps femoris and hamstring muscles has been found to enhance the response of both muscles to phasic stretch.23'24 In similar studies involving muscles of the upper extremity, the phasic stretch reflex of the triceps brachii muscle is enhanced by length in normal, hemiplegic, athetoid, and parkinsonian subjects.20,22,23 However, the phasic stretch reflex of the biceps bra chii muscle is facilitated by length in parkinsonian and hemiplegic subjects, yet is inhibited by length in normal and athetoid subjects.23'25'26 The reasons for these differences between various patients are not
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II afferent-fiber discharge appeared to produce a monosynaptic excitation of the internal intercostal alpha motoneurons. Subsequent investigations, using similar techniques, have also revealed a monosynaptic excitation of alpha motoneurons of the triceps surae muscle by group II afferent fibers from that muscle.20 These are remarkable observations, because up to this time the only monosynaptic spinal reflex thought to exist was that evoked by the la afferent fibers from the muscle spindle. As should be obvious from the above experiments, it is not appropriate to describe the reflex action of the group II afferent fibers of the muscle spindle as being only excitatory to flexor muscles and inhibitory to extensor muscles. Rather, several different reflex actions have been found to be possible, depending in part on the animal preparation. One explanation for the diverse reflex actions is that the predominant reflex action of these group II afferent fibers is me diated by interneurons in the spinal cord. The activity of spinal interneurons is greatly influenced by su praspinal input in the normal nervous system. If supraspinal centers are damaged, the activity of spinal interneurons can be dramatically altered. Interneu rons mediating reflexes of group II afferents can be
PHYSICAL THERAPY
clear; alterations in the reflex actions of the group II afferent fibers may be involved.
1. Stockmeyer SA: An interpretation of the approach of Rood to the treatment of neuromuscular dysfunction. Proceedings: An exploratory and analytical survey of therapeutic exercise, Northwestern University. Am J Phys Med 46:900-961,1967 2. Lloyd DPC: Integrative pattern of excitation and inhibition in two-neuron reflex. J Neurophysiol 9:439-444, 1946 3. Eccles RM, Lundberg A: Synaptic actions in motoneurons by afferents which may evoke the flexion reflex. Arch Ital Biol 97:199-221, 1959 4. Wilson VJ, Kato M: Excitation of extensor motoneurons by group II afferent fibers in ipsilateral muscle nerves. J Neu rophysiol 28:545-554, 1965 5. Kuno M, Perl ER: Alteration of spinal reflexes by interaction with suprasegmental and dorsal root activity. J Physiol 151: 103-122, 1960 6. Matthews PBC: Evidence that the secondary as well as the primary endings of the muscle spindles may be responsible for the tonic stretch reflex of the decerebrate cat. J Physiol (Lond) 204:365-393, 1969 7. Matthews PBC: Mammalian Muscle Receptors and Their Central Actions. London, Edward Arnold Ltd, 1972, pp 421423 8. Bianconi R, Vander Meulen JF: The response to vibration of the end-organs of mammalian muscle spindles. J Neuro physiol 26:177-190, 1963 9. Brown MC, Engbert I, Matthews PBC: The relative sensitivity to vibration of muscle receptors of the cat. J Physiol 192: 773-800, 1967 10. Granit R: Neuromuscular interaction in postural tone of the cat's isometric soleus muscle. J Physiol 143:387-402,1958 11. Grillner S: Is the tonic stretch reflex dependent upon group II excitation? Acta Physiol Scand 38:431-432, 1970 12. Rack PMH, Westbury DR: The effects of length and stimulus rate on tension in the isometric cat soleus muscle. J Physiol 204:443-460, 1969 13. Cook WA, Duncan CC: Contribution of group I afferents to the tonic stretch reflex of the decerebrate cat. Brain Res 33: 509-513, 1971 14. Matthews PBC: A reply to criticism of the hypothesis that the group II afferents contribute excitation to the stretch reflex. Acta Physiol Scand 79:431-433, 1970
15. Matthews PBC: A critique of the hypothesis that spindle secondary endings contribute excitation to the stretch reflex. In Stein RB, Pearson KG, Smith RS, et al: Control of Posture and Locomotion. New York, Plenum Press, 1973, pp 227243 16. McGrath GJ, Matthews PBC: Evidence from the use of vibra tion during procaine nerve block that the spindle group II fibres contribute excitation to the tonic stretch reflex of the decerebrate cat. J Physiol 235:371-408, 1973 17. Westbury DR: A study of stretch and vibration reflexes of the cat by intracellular recording from motoneurones. J Physiol 226:37-56, 1972 18. Fromm C, Haase J, Wolf E: Depression of the recurrent inhibition of extensor motoneurons by the action of group II afferents. Brain Res 120:459-468, 1977 19. Kirkwood PA, Sears TA: Monosynaptic excitation of moto neurones from secondary endings of muscle spindles. Nature 252:243-244,1974 20. Kirkwood PA, Sears TA: Monosynaptic excitation of moto neurones from muscle spindle secondary endings of inter costal and triceps surae muscles in the cat. J Physiol 245: 64-65P,1975 21. Burke P, Gillies JD, Lance JW: The quadriceps stretch reflex in human spasticity. J Neurol Neurosurg Psychiatry 33:216223, 1970 22. Burke P, Gillies JD, Lance JW: Hamstrings stretch reflex in human spasticity. J Neurol Neurosurg Psychiatry 34:321325, 1971 23. Andrews CJ, Neilson P, Knowles L: Electromyographic study of the rigidospasticity of athetosis. J Neurol Neurosurg Psy chiatry 36:94-103, 1973 24. Andrews CJ, Burke D, Lance JW: The response to muscle stretch and shortening in parkinsonian rigidity. Brain 95: 795-812, 1972 25. Ashby P, Burke D: Stretch reflexes in the upper limb of spastic man. J Neurol Neurosurg Psychiatry 34:765-771, 1971 26. Andrews CJ, Neilson PD, Lance JW: Comparison of stretch reflexes and shortening reactions in activated normal sub jects with those in Parkinson's disease. J Neurol Neurosurg Psychiatry 36:329-333, 1973
CLINICAL IMPLICATIONS
Volume 59 / Number 9, September 1979
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A basic message of this review is that the group II afferent fibers of the muscle spindles can exert diverse reflex actions, depending upon the integrity and state of the CNS. Thus, the reflex action of these fibers may vary widely in the neurologically involved pa tient. Therapists have attempted to use the classical reflex of flexor facilitation and extensor inhibition attributed to these afferent fibers, yet these actions may be manifested primarily in patients with spinal cord injury and may not even exist in the majority of
patients with brain damage. At the present, more experimental work needs to be done to define clearly the reflex action of the group II afferent fibers from the muscle spindle in patients with a neurological deficit. Physical therapists should be aware that pa tients with a particular brain deficit may have one type of reflex from activation of the group II afferent fibers from muscle spindles while patients with an other brain lesion may have a different response. At this time, specific brain lesions cannot be definitely associated with specific reflex actions of the group II afferent fibers. Therefore, therapists should be cau tious in making and accepting statements about the reflex action of these fibers in patients with brain damage until experimental evidence has been thor oughly developed.
