The Neuropnysiology of Tone: The Role of the and the

The excitability of the stretch reflex is used as HELEN CAMERON-TUCKER a measure of tone. The muscle spindle is the receptor for the stretch reflexes which may be Helen Cameron-Tucker, B Phty\(Hons.), is a Senior Tutor in the Department of Physiotherapy, University phasic or tonic in nature. This paper provides of Queensland. a theoretical background through an overview of published studies as a basis for the under• standing of the contribution of the muscle spindle to both the phasic and tonic stretch reflexes.

Physiotherapists are concerned with reflex contraction. This reflex firing organ lies, a phenomenon described the analysis of movement One of the of motor units occurred in the absence by Ganong (1973) as the 'inverse factors involved in governing normal of other afferent stimulation and led stretch reflex' or autogenetic inhibi• movement is normal muscle tone, one Magoun and Rhmes (1947) to conclude tion. These events, depicted diagram- definition of which is presented by that a muscle must contain its own matically m Figure 1, occur because Wyke (1976) as being the tension stretch receptors which discharge via the Golgi organ with obtaining at any one moment between afferents into the . The an inhibitory interneurone which in the origin and insertion of each mus• reflex excitation of alpha motor neu• turn synapses with and inhibits the cle. Tone is assessed clinically by rones results in the firing of motor anterior horn cell of the agonist. At testing and observing the excitability units and finally the muscle contrac• the same time, reciprocal excitation of of the phasic and tonic stretch reflexes, tion observed by Liddell and Sher- the antagonistic muscle occurs (Gan• An understanding of the normal neu- nngton (1924). ong 1973). rophysiological basis of these reflexes The stretch sensitive receptors in Ganong (1973) stated that via au• is necessary if the pathological behav• muscle are now known to be the Golgi togenetic inhibition, the Golgi tendon iour is to be appreciated. tendon organ and the muscle spindle, organ has a protective function in that both of which have different rates. if the tension in a contracting muscle Stretch Receptors in Muscle The muscle spindle is responsible for becomes too great the receptor is Wyke (1976) presents a triad of reflex contraction of the homonymous activated, causing the muscle to sud• mechanisms which determine muscle muscle, whereas the Golgi tendon or• denly relax, and thus reducing the tone or tension: elastic properties of gan acts to inhibit the homonymous tension to safer levels. Jansen and , muscles and the connective reflex . (Fulton Rudjord (1964) found that the amount tissue of fascial sheaths and intramus• 1943, Eldred 1965, Matthews 1968, of active muscular tension required to cular septa; visco-elastic properties of Matthews 1973). excite tendon organs is small in rela• fibrillary protein in each muscle fibre; tion to the potential strength of the and the degree of activity. whole muscle and this led Matthews As motor unit activity is influenced The (1973) to abandon the hypothesis that by the excitability of the nervous The Golgi tendon organ has been Golgi tendon organs have a purely system, it is this determinant which is described as being a collection of nerve protective role. Matthews (1973) also capable of wide variation and is of endings lying in series with the extra- noted that Golgi tendon organs can paramount importance in the regula• fusal muscle fibres at the musculo- be excited by single motor units and tion of muscle tone. tendinous junction at each end of the therefore may be excited by only the The firing of a motor unit occurs muscle. Due to this 'in series' arrange• muscle fibres attaching to the tendon in response to a stimulus acting upon ment, stretch of the muscle fibres and on which the organ lies and not by the alpha motor neurone in the ventral therefore the tendon to which the other fibres. The Golgi tendon organ of the spinal cord (Ganong fibres attach, activates the Golgi ten• would then sample the contraction 1973, Barr 1972). Liddell and Sher- don organ. (Eldred 1965, Ganong rather than taking a widespread av• nngton's (1924) experiments on decer- 1973, Matthews 1973). erage. Matthews (1973) concluded that ebrate cats demonstrated that a muscle Stimulation of this receptor causes the Golgi tendon organ functions as responds to a stretch stimulus with a relaxation of the muscle in which the a contraction receptor, playing a con-

The Australian Journal of Physiotherapy Vo! 29, No 5, October, 1983 155 The Neurophysiology of Tone

a similar structure, as depicted in Figure 2. Golgi -<

156 The Australian Journal of Physiotherapy Vol 29, No 5, October, 1983 The Neurophysiology of Tone

traction. Dynamic nuclear bag fibres (DNB) have a slow time course of contraction, whereas static nuclear bag fibres (SNB) have a fast time course. This could indicate that the energy requirements of DNB fibres are less than those of the SNB fibres, and that perhaps the DNB fibres are equivalent to the bag 1 fibres and the SNB fibres to the bag 2 fibres. Support for this conclusion has been given by Laporte (1979) in a review of the work of physiologists in this area The majority of bag 1 fibres (or DNB fibres) respond to stimuli from dynamic efferents whereas bag 2 (SNB) fibres respond to static stimuli (Laporte 1979). Coupled with the lower energy requirements and slower time course of contraction, this sug• gests that DNB fibres participate in the reflex control of dynamic or phasic movement On the other hand, SNB Dynamic Static Nuclear Nuclear Nuclear Cham fibres which have higher energy re• Bag Bag Fibre Fibre Fibre quirements and a fast time course of contraction appear to be involved in Figure 2- Structure of the muscle spindle (Adapted from Korten, 1972) eliciting static or tonic muscle activity.

Mi c/ear Cham Fibres The small intrafusal fibres identified by Boyd (1956) have their central nuclei lying in a single file or chain in 1973) The mitochondria are therefore other muscle protein, actomyosin re• the central region, with a few nuclei concentrated in areas where energy sults. Actomyosm is the unique com• at the poles, and are known as nuclear requnements are high, and as ATP plex responsible for the contractile chain (NC) fibres (Matthews 1973). ase is involved in the energy producing properties of muscle fibres (Ganong These fibres are attached to the con• reactions, it too is concentrated in 1973) According to Barker ef al nective tissue capsule of the spindle; structures requiring large amounts of (1976), the appearance of an M line that is to say, they are intracapsular energy It is therefore not surprising in intrafusal fibres is accompanied by (Eldred 1965). that Barker, Banks, Marker, Millburn increased mitochondria, increased sar- According to Barker ef al (1976), and Stacey (1976) found that bag 1 coplasm between , and a the nuclear chain fibres have high fibres which have a low ATP ase better developed sarcotubular system, staining for ATP ase, possess a well- staining reaction possess few mito• all of which indicate increased energy developed M line, prominent mito• chondria requirements or muscle fibre activity. chondria, increased interfibrillary sar- Barker ef al (1976) also found that From this it can be deduced that bag coplasm, and a well-developed sarco• bag 1 fibres often lack an M line 1 fibres (which often do not possess tubular system. Nuclear chain fibres (although one may be present in the an M line) and bag 2 fibres (which do also have more glycogen than do bag poles), whereas bag 2 fibres have an possess an M line) differ in terms, of 2 fibres which, in turn, have more M line throughout except in the area energy requirements and therefore glycogen than bag 1 fibres. (Glycogen adjacent to the bag region. M lines function. Boyd (1976) has found this is the substance utilized in the pro• are dark zones found in the middle of to be the case duction of ATP, and is therefore part an A band which corresponds to Boyd (1976) differentiated two types of the energy producing cycle (Ganong , a muscle protein When of nuclear bag fibres by studying the 1973).) This suggests that the energy myosin is combined with , an• nature and time course of their con- requirements of NC fibres are high,

The Australian Journal of Physiotherapy Vol 29, No 5, October, 1983 157 The Neurophysiology of Tone

and appear to be similar to those of is now called, is located on nuclear (velocity) sensitivity of the primary SNB fibres. The similar energy re• bag and chain fibres, whereas the ending is not surprising when it is quirements and the demonstration that flower spray or secondary receptor is considered that the receptor is found NC fibres as well as SNB fibres re• found only on NC fibres. coiled around the less viscous equator spond to static stimuli (Boyd, Glad• of the intiafusals where the resistance den, McWiIham and Ward 1975) in• Primary Ending and Group la to stretch is less In addition, the dicates that NC fibres participate with Afferent primary ending is found on the bag 1 SNB fibres in reflexly controlling tonic Each muscle spindle has only one (DNB) fibres which respond to dy• muscle activity primary ending, branches of which namic stimuli and is also coiled around coil around every intrafusal fibre. This the bag 2 (SNB) and NC fibres which Tandem Spindles sensory ending is continuous with a respond to static stimuli. Muscle spindles usually have both single large myehnated rapidly con• (b) Discharge Pattern nuclear bag (DNB and SNB) and ducting la afferent which is 12- A study of the discharge pattern of nuclear chain fibres, although spindles 20 pun in diameter (Eldred 1965, Mat• the primary ending also reveals its with only one type of nuclear bag thews 1973). dynamic (phasic) and static (tonic) fibre have been found (Barker et al sensitivity At the beginning of muscle 1976). Cooper and Daniel (1963) (a) Location and Sensitivity to Stretch stretch, the primary ending shows a found that the human lumbncal mus• The primary ending spirals round burst of discharge (phasic activity) cles have only nuclear bag fibres the central equatorial region of the which gradually falls to a steady main• whereas Cooper et a7 (1955) reported intrafusal fibres where they lose their tained level (tonic activity) appropriate that human extraocular intrafusals striatiorts and appear to be non-con• to the new length of the muscle (Eldred rarely have a nuclear bag formation tractile and offer less viscous resistance and Tokizane 1955) Matthews (1973) Barker and Gidumal (1961) reported to stretch (Eldred 1965, Matthews claimed that the primary ending can the presence of transitional forms of 1973). Some of the nuclear bag fibres 'reset' itself so that its high sensitivity mtrafusal muscle fibres where a bag on which primary endmgs are located to stretch transfers itself to a new fibre in one spindle continued through are percapsular, passing beyond the muscle length, preventing the endings to the next spindle as a chain fibre. connective tissue capsule of the spindle from becoming saturated Szumski Boyd (1960) wrote that true tandem to attach to tendon and . (1974) added that when the stretch is spindles with continuous intrafusal These attachments, if stretched, would released (or a muscle relaxes), the fibres are rare, although spindles may directly stretch the primary ending fibres recoil (or lengthen) and the have overlapping ends. However, Bar• whether or not the muscle spindle had primary ending again discharges ker et al (1976) discovered in one of been stretched. This means a similar (phasic activity) during this movement their experiments a tandem spindle degree of external stretch is needed to Eldred and Tokizane (1955) noted that with a bag 1 (DNB) fibre continuing activate the primary ending (Eldred there is a pause in primary firing in the next spindle as a NC fibre. The 1965) Hunt (1955) has found the following release of passive stretch or functional significance of tandem threshold value of stretch needed to cessation of muscle contraction spindles remains unclear. activate primary endings in soleus muscle to be 3 gms. As Eldred (1965) (c) Central Connections Sensory Endings and Afferents pointed out, this sensitivity to small The information about the stretch Eldred (1965) presented four criteria changes in tension is important be• of a muscle is conveyed by the la to be considered in the classification cause a muscle is capable of changing afferents to the central nervous sys• of muscle spindle afferents. These are length considerably without altering tems (CNS) In the CNS there are the number of sensory endings present tension very much. If the primary supraspinal pathways and spinal cord m the spindle, the position of the ending was not extremely sensitive to connections. The supraspinal pathway ending along the length of the intra• stretch, this change in muscle length is the dorsal fusal fibre, the structure of the ending, at low tensions would go unnoticed. which activates the and and the size of its axon. With this in Matthews (1973) discussed the sensi• utimately influences muscle tone via a mmd, the sensory endings and their tivity of the primary ending to stretch, cortico-cerebellar-cortical loop and afferents may be divided into two noting that not only is it sensitive to then via the descending cortico-spinal groups. Ruffini (1897) described two change in length of the muscle, but it tracts (Noback 1967, Barr 1972) types of sensory ending — an annu- shows a high sensitivity to the velocity At a spinal cord level, the la afferent lospiral and a flower spray ending. at which the stretching occurs. has a monosynaptic facihtatory syn• Boyd (1956, 1957) noted that the This static sensitivity (responsive• apse with the anterior horn cell (alpha annulospiral, or primary ending as it ness to change in length) and dynamic motoneurone) of the muscle in which

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the spindle is located (in this expla• McLeod 1975). The dynamic sensitiv• toneurones, rendering it significant in nation the homonymous muscle is ity of the primary ending, the phasic the maintenance of muscle tone by teimed the agonist), a polysynaptic nature of its discharge, its continua• the tonic firing of motor units. facihtatory with the alpha tion with the rapidly conducting ia In summary, the primary ending motoneurones of the agonist or sy- afferent fibres which monosynapti- and Ia afferent of muscle spindles is nergist, and a disynaptic inhibitory cally excite alpha motoneurones, and both a dynamic and a static receptor, synapse with the alpha motoneurones its location on dynamic nuclear bag controlling muscle tone via the mono• of the antagonist (Ganong 1973, fibies indicate that the primary ending synaptic phasic stretch reflex and the Scholz and Campbell 1980) Interneu- of muscle spindles is the receptor polysynaptic tonic stretch reflex. rones mediate the la facilitation and involved m the reflex control of phasic the la reciprocal inhibition in the poly- muscle activity. Secondary Ending and Group II and disynaptic pathways respectively The tonic stretch reflex, on the other Afferents and are themselves influenced by the hand, is one in which a stimulus The second afferent from muscle descending supraspinal pathways produces a prolonged asynchronous spindles reminded Ruffini (1897) of a (Hultborn 1976). These central con• discharge of motor neurones causing wreath of flowers because of its struc• nections of the primary ending and its sustained muscle contraction for the ture. It was historically known as the la afferent are depicted diagrammat- maintenance or alteration of posture. 'flower spray' receptor but is now lcally in Figure 3. The length of the time course is such referred to as the secondary ending. The reflex response of muscle to that more than one synapse has been According to Matthews (1973), the stretch has also been found to be suggested. That is to say, it is poly• structural difference between the pri• phasic or tonic in nature. Lance and synaptic. Clinically, this reflex is elic• mary and secondary ending is well McLeod (1975) defined the phasic ited by passively stretching a muscle marked in the cat but not in man. stretch as a synchronous motor neu• (Lance and McLeod 1975). The pri• Under the electron miscroscope, both rone discharge caused by a brief stim• mary ending is also activated by human spindle receptors are closely ulation of muscle spindles or their change in length per se of muscle applied to the intrafusal muscle mem• afferent nerve pathways. This reflex fibres (static sensitivity), is located on brane and appear the same except for is seen clinically as the tendon jerk. SNB fibres and NC fibres, may dis• their size. The time course is such that the reflex charge tonicaliy, and has polysynaptic There are usually from one to five must be monosynaptic (Lance and facihtatory synapses with alpha mo- secondary endings per spindle, al• though some small spindles have been found not to contain any. When sev• eral secondary endings are present, each is continuous with its own affer• Descending ent axon, but endings in nearby muscle Supraspinal spindles may join the axon of an To Cerebellum Influence ending from another spindle (Eldred A 1965). Supraspinal Eldred (1965) explained that the Level secondary endings are continuous with Spsnal Level the myehnated group II afferent which have a diameter of 4-12^. As -<♦- -<0- the group II fibres have a smaller amn To Antagonist diameter than the group la afferents, their nerve conduction velocity is slower (Erlanger and Gasser 1924). r~<4 (0- To Synergtst or Agonist (a) Location and Sensitivity to Stretch 6- «h Boyd (1957) found that secondary Primary Endtng To Agonist endings are located on nuclear chain and fa Afferent fibres, lying on either side of the —^ inhibitory primary ending; that is, lying juxta- —^ facihtatory mterneuron equatorially. Hunt's (1954) experi• amn alpha ments showed that the threshold for stretch for soleus muscle secondary Figure 3: Diagrammatic representation of la afferent projections endings is 19 gms. This is much higher

The Australian Journal of Physiotherapy Vol 29, No 5, October, 1983 The Neurophysiology of Tone

than that of the primary ending, in• tonic discharge. This suggested to such as Matthews (1969) and Kanda dicating that the secondary ending is Eldred (1965) that the secondary end• and Rymer (1977) whose studies with not as sensitive to stretch as the dy• ing behaves as a receptor of little vibration and muscle stretch showed namic primary ending. Eldred (1965) adaptation and exhibits greater static that simultaneous vibration and noted that the location of secondary or tonic sensitivity than does the dy• stretch of a muscle did not result in endings on nuclear chain fibres con• namic or phasic primary ending. (It the one occluding the other, but rather tributes to its lower stretch sensitivity. must be remembered, however, that an increase in muscle tension which The nuclear chain fibres are intracap- the primary ending has static as well was greater than that produced by sular, attaching to the connective tis• as dynamic sensitivity. To Eldred vibration or stretch alone. This led sue capsule of the spindle. According (1965) this indicated that the primary these authors to conclude that as the to Eldred (1965), this means that the ending behaves as a dual receptor, la afferent discharge was held constant secondary endings would be affected showing slow (static) adaptation or by vibration, the observed increase in by extrafusal muscle stretch only if rapid (dynamic) adaptation, depend• muscle tension with vibration and this first lengthened the capsule. Fur• ing on the nature of the muscle stretch must be due to activation of thermore, the juxtaequatorial region stretch.) the secondary endings by the stretch. of the nuclear chain fibres where According to Matthews (1969), these secondary endings are located is mod• (c) Central Connections findings suggest a role for the second• erately well striated, offering more Like the primary afferent, the group ary endings together with the primary viscous resistance to stretch. Boyd II axons convey information to the ending in producing the tonic stretch (1976a) noted that in the juxtaequa• central via spinal and reflex. torial region, the nuclear chain fibres supraspinal pathways. The secondary The hypothesis that the secondary have 'kinks'. A greater degree of afferent projects with the primary endings function with, and augment, stretch would therefore be required to afferent to the cerebellum via the the primary ending discharge, is sup• stretch out these kinks and activate dorsal spino-cerebellar tract. At a ported by the experimental work of the secondary endings. spinal level, the reflex connections are Chapman, Michalski, and Siguin The higher threshold to stretch of different from those of the primary (1979). Their work showed that 65 per the secondary ending indicates that it afferent and controversy exists as to cent of group II afferents gave an is not so much the rate or velocity of the exact control the secondary ending excitatory input to extensor motoneu• stretch which activates the receptor, has over muscle tone via its synapses rones — a direct contradiction to the but the amount of stretch or change in the spinal cord. classical concept of group II afferent in length of the muscle fibre. Matthews The classical concept of group II function. The remaining 35 per cent (1973) reported this to be the case, afferent action on motoneurones arose of group II afferents behaved in stating that the greater sensitivity of from the experimental work of people accordance with the classical con• the secondary ending to change in such as Lloyd (1946) who found that cept and were inhibitory to extensor length per se of the muscle fibre in spinal cats stimulation of the group motoneurones. Chapman and his col• renders it a static receptor. II afferents facilitated flexor muscles leagues (1979) concluded that the sec• and inhibited extensors on the same ondary endings may not be a func• (b) Discharge Pattern (ipsilateral) side of the body, regard• tionally homogenous group and that Examination of the discharge pat• less of the muscle in which the reflex under normal circumstances the ma• tern produced by secondary endings originated. Due to its long central jority (65 per cent) of secondary end• in response to stretch further indicates latency the reflex was thought to be ings reinforce the primary ending. the static nature of this receptor. When polysynaptic, the effects being med• However, in cases of neurological dys• activated, secondary endings show a iated by interneurones. function such as spinal cord injury greater discharge per change in unit Burke and Lance (1973) studied the where there is little or no descending length than do primary endings. At a reflex effects of group II afferents in facilitation of extensor motoneurones, constant muscle length secondary end• human subjects and their results agree the action of the remaining 35 per ings fire more regularly than primar• with those of Lloyd (1946). Burke and cent of secondary endings may become ies. That is, secondary endings exhibit Lance (1973) concluded that the facil• apparent — that is, ipsilateral facili• a tonic discharge (Matthews 1973). itation of hamstrings (flexor) activity tation of flexors and inhibition of Eldred and Tokizane (1955) reported and the inhibition of quadriceps (ex• extensors. that following release of passive tensor) activity in spastic human sub• Matthews (1969) also considered stretch or muscle contraction, second• jects was due to activation of the that the effects of secondary ending ary endings (in contrast to primary secondary ending by stretch. This view stimulation might depend upon the endings) show barely any pause in has been challenged by researchers integrity of the CNS. As Matthews

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(1969) observed, interneurones me• especially that of antigravity postural spond to a functional classification diate reflex effects of secondary end• muscles, via the tonic stretch reflex. based on the response of the primary ings. Interneurones are susceptible to The remainder of secondary endings ending to stretch (Matthews 1973), descending supraspinal influence and, facilitate flexor tonus and inhibit ex• Matthews (1962) found that stimula• in Matthews' (1969) opinion, may be tensor tonus on the ipsilateral side tion of gamma 1 (plate) efferents 'switched on or off following CNS regardless of the muscle in which the increased the dynamic (velocity) re• damage. If those mediating autoge- reflex originated These effects are sponse of the primary ending to netic excitations were 'switched on', mediated by mono- or polysynaptic stretch. Stimulation of the gamma 2 then the reflex effect of secondary pathways and their expression ulti• (trail) ending decreased the primary ending stimulation by stretch would mately depends upon the function and ending velocity sensitivity whilst in• be facilitation of the muscle activity. integrity of the CNS, which facilitates creasing its static response. The two That is, the secondary ending would or inhibits interneurones m the poly• kinds of fusimotor fibres are now reinforce the action of the primary synaptic pathway. named dynamic or static efferents and ending. On the other hand, if the correspond to the gamma 1 or gamma interneurones to extensor muscles were Efferents: of the 2 fibres respectively (Matthews 1973). 'switched off* then the group II af• Muscle Spindle Eldred (1965) discussed the contro• ferent would reflexly inhibit extensors The mtrafusal fibres of the muscle versy as to whether the dynamic and whilst facilitating flexors. Matthews spindle have been found to have their static gamma efferents supply a dis• (1969) concluded that this concept of own nerve supply (Boyd 1961). If these tinct type of mtrafusal fibre. Earlier group II fibre reflex effects allows for motor efferents influence the excita• experiments (Boyd 1961) indicated that a graded control of muscle tone from bility of the muscle spindle stretch dynamic efferents supplied nuclear bag excitation to inhibition via the tonic receptor, then they could well be in• fibres and static efferents ended on stretch reflex. In a review of the volved in the reflex control of tone. nuclear chain fibres. Barker (1962) literature, Urbscheit (1979) and Mun- The efferents to striated muscle arise disputed this, stating that gamma ef• son, Fieshman and Sypert (1980) from motoneurones located in the ferents are not restricted to one type agreed that the secondary endings are anterior or ventral horn of the gray of mtrafusal fibre and indeed one involved in the tonic excitation of matter of the spinal cord. They may mtrafusal fibre may carry both types antigravity musculature — often ex• be divided into two groups: the effer• of efferent. tensors — and have a diverse effect ents which are greater than 12ptm in Later experiments by Boyd et al upon muscle tone, depending upon the diameter, arise from large alpha mo• (1975) demonstrated that whereas dy• integrity of the CNS. toneurones, and supply extrafusal namic gamma efferents innervate DNB The polysynaptic nature of the muscle fibres; and the smaller (8-12^m fibres, cross innervation exists between group II fibre reflex pathway was in diameter) gamma efferents inner• SNB and NC fibres. When the similar challenged when Kirkwood and Sears vating the mtrafusal fibres (Matthews function of the SNB and NC fibres is (1974) demonstrated in cats that af• 1973). Eccles, Eccles, Iggo and Lund- considered, it is not surprising to find ferent impulses arising from group II berg (1960) found that the gamma that both are innervated by static fibres monosynaptically excite moto• motoneurones of a muscle are located gamma efferents. Laporte's (1979) re• neurones. This monosynaptic pathway within the nucleus of alpha motoneu• view of the literature on this subject for secondary endings does not mean rones supplying that muscle. They give showed support for the experiments that they are involved in the mono• rise to the gamma efferent, also known of Boyd et al(\915) and also presented synaptic stretch reflex (MSR) or ten• as the fusimotor fibre. As Matthews evidence to suggest that some DNB don jerk because, as Matthews (1964) (1973) pointed out, the separation of fibres are also innervated by static pointed out, the secondary endings are fusimotor from skeletomotor control gamma efferents. However, as Mat• not excited by the small rapid stretch is not always distinct and a shared thews (1973) stated, the nuclear bag of a muscle used to elicit the MSR fusimotor-skeletomotor innervation and nuclear chain fibres appear to whereas the primary endings are. (known as the beta fibre) has been have sufficient distinct motor inner• It appears that the control of tone found. vation to result in distinct dynamic by the secondary endmg/group II af• Boyd (1961) described two types of and static motor effects, resulting in ferent is complex. The recent data fusimotor fibres: the gamma 1 fibres a degree of independent reflex control suggests that these receptors are not a which ended in plates on nuclear bag of muscle activity. functionally homogenous group. Part fibres; and the gamma 2 fibres which of the population of secondary endings had diffuse trail like endings on nu• Dynamic Gamma Efferents reinforce the action of the primary clear chain fibres. This histological The dynamic gamma efferents (2.5- ending in influencing muscle tone, separation has been found to corre• 4.0/^m) terminates on the DNB fibres

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in discrete plate endings (Boyd 1961). are smaller than the dynamic gamma been seen to be the receptors of the The gamma plate endings lie towards efferents they have a slower nerve tonic stretch reflex As the firing of the poles of the spindle and several conduction velocity (Erlanger and these receptors is regulated by static may lie on any one nuclear bag fibre. Gasser 1927). gamma efferent discharge, the static The plate endings often arise from Although it was classically thought gamma motoneuron with its efferent separate dynamic fusimotor fibres al• that static gamma efferents innervated is important in the maintenance of the though one efferent may branch to NC fibres only, subsequent research tonic stretch reflex and therefore in supply several plate endings (Matthews in this area has shown that this appears the control of muscle tone. 1973). Barker, Stacey and Adal (1970) not to be so. Boyd et al (1975) ob• have further subdivided the plate end• served static efferents terminating on Beta Efferents ings into 'p,' and 'p2' plates, the p, SNB as well as NC fibres. Barker Adal and Barker (1965) observed plates closely resembling the motor (1976) agreed with the observations of individual motor fibres which end plates on extrafusal fibres. Barker Boyd et al (1975), adding that bag 1 branched to supply both intrafusal et al (1970) found that while a bag 1 (DNB) fibres also have some inner- and extrafusal fibres These collaterals (DNB) intrafusal fibre always had a vation by static efferents. Laporte's of alpha efferents, known as beta p2 plate, bag 2 (SNB) and NC fibres (1979) review on the intrafusal distri• fibres, are intermediate in size between may also occasionally have a p, plate. bution of dynamic and static fusimo• alpha and gamma fibres (Laporte and These authors found that 90 per cent tor fibres concluded that about one- Emonet-Denand 1976). Based on the of p2 plates ended on nuclear bag third of DNB intrafusals are inner• work of Erlanger and Gasser (1927) fibres and 10 per cent on chain fibres. vated by static gamma efferents. As the beta fibres have a nerve conduction On this basis, stimulation of the Laporte (1979) wrote, Emonet-Den- velocity between alpha and gamma gamma plate (dynamic) efferents ard, Laporte, Matthews and Petit fibres. would result in contraction of DNB, (1977) suggested that the innervation SNB and NC fibres. The primary of DNB fibres by static efferents could The presence of beta fibres has been ending coils around all intrafusal preserve their responsiveness to stretch well documented in amphibian (Katz fibres, and would therefore be influ• when the dynamic system is not active 1946), reptilian (Proske 1969) and enced by the dynamic gamma efferent. as would be the case during strong mammalian muscle spindles (Bessou, (Secondary endings also lie on NC static stimulation. According to Mat• Emonet-Denand and Laporte 1965; Emonet-Denand, Jamie and Laporte fibres and are, according to Matthews thews (1973), the secondary endings 1975; and Boyd, Gladden, McWilliam (1973), controlled exclusively by static on NC fibres respond only to static and Ward 1977). Beta fibres to mam• gamma efferents. Dynamic efferents efferent stimulation. Matthews (1973) malian muscle spindles have been excite only the primary endings). Dy• argued that the strong static effects found to terminate on both nuclear namic gamma fusimotor discharge resulting from the simultaneous exci• bag and nuclear chain intrafusal fibres controls the velocity sensitivity of the tation of NC and SNB fibres would (Barker, Emonet-Denand, Harker, primary ending to stretch (Matthews mask the effects of stimulatng the Jamie and Laporte 1976; Boyd et al 1973), Via the primary ending con• DNB fibre. 1977). nections with the alpha motoneurones, It appears that the major effect of the dynamic fusimotor fibres are static gamma discharge arises from the Primary endings have been seen to therefore involved in controlling the SNB and NC fibres, resulting in ex• spiral around the three types of intra• sensitivity of the phasic stretch reflex. citation of the primary (static sensitiv• fusal fibre and contraction of these ity) and secondary endings. Continu• fibres by beta efferents would result Static Gamma Efferents ous or tonic firing of these receptors in stimulation of the primary receptor. Boyd (1961) decribed a diffuse end• is brought about by the repeated firing It is Post, Rymer and Hasan's (1980) ing from gamma 2 (static) efferents of the static gamma motoneuron. The view that beta efferents, by providing on nuclear chain fibres. Barker, Stacey gamma motoneuron has many mter- an additional means of spindle exci• and Adal (1970) named these termi• neurones impinging on it. Via these tation, would ensure continued stim• nations 'trail endings'. In contrast to interneurones the descending supra- ulation of intrafusals if fusimotor ac• the plate endings, the trail endings spinal tracts (such as vestibulospinal tivity is largley completed before the have no discrete point of termination. or reticulospinal tracts) are able to threshold for extrafusal contraction Instead, they are spread along the influence and maintain the tonic dis• has been reached. Beta activity there• intrafusal fibre, lying on the juxta- charge of the gamma motoneuron fore increases la afferent discharge on nuclear portion. The static gamma (Barr 1972). a background of gamma motoneuron efferents are 1.2-2.Q^m in diameter Primary endings on SNB fibres and activity, constituting a positive means (Matthews 1973). As the static fibres secondary endings on NC fibres have of excitation for muscle spindles.

162 The Australian Journal of Physiotherapy Vol 29, No 5, October, 1983 The Neurophysiology of Tone

Phasic and Tonic Motor Units lism produces high levels of energy, motor unit type occurs even with making the 'red' fibres well suited for muscles which are supplied by an It has been seen that the muscle tonic work. Conversely, the fast twitch admixture of 'fast' and 'slow' moto• spindle exerts dynamic/phasic or or 'pale' fibres which are low in neurones; that is, muscles which are static/tonic control over muscle activ• oxidative enzymes (Kugelberg and Ed• involved in both phasic and tonic ity In 1956, Granit, Henatsch and strom 1968) are easily fatigued and activity. Steg, followed by Granit, Phillips, are suited for short bursts of phasic Skoglund and Steg (1957), demon• or dynamic activity (Edstrom 1973). strated that the alpha motoneurones It would be reasonable to assume The Phasic and Tonic Stretch in the ventral horn could be divided that slow 'red' motor units which fire Reflexes into two functionally different groups: tonically would be innervated by The differentiation between tonic phasic and tonic. Phasic alpha moto• efferents arising from tonic alpha and phasic function has been seen at neurones responded only briefly to a motoneurones and that phasic alpha a motoneuron, muscle spindle, and tetanizmg stimulus whereas tonic mo• motoneurones would supply fast 'pale1 extrafusal fibre level. Muscle spindle toneurones showed a repetitive long motor units Eccles, Eccles and Lund- discharge can be evoked in two ways lasting discharge following the stimu• berg (1958) found this to be the case. One way is by stretching the tendon lus. The efferent axon of the phasic These authors added that the corre• or the extrafusal fibres to which the motoneuron was found to be larger spondence between motoneuron and tendon attaches and so imparting the in diameter than the tonic axon Ac• cording to the nerve conduction' ve• locity studies of Erlanger and Gasser (1927), the phasic axon would have a Anterior Horn of faster nerve conduction velocity This Spinal Cord Descending f Supraspmal is in keeping with the faster dynamic Influence muscle contraction resulting fiom / phasic motoneuron discharge. In Rushworth's (1964) opinion, it is likely that in man, phasic motoneurones are involved in the tendon jerks or mono- synaptic stretch reflex and tonic 11 motoneurones in the maintenance of Tonic Phasic posture via the tonic stretch reflex. omn The muscles themselves have been Dynamic and Static yrnn found to be made up of two func• Phasic and Tonic Alpha Efferents tionally different types of fibres. Ec- _J3 £ cles, Eccles and Lunderg (1958) re• ported on the experimental work of Ranvier, 1874, and Kronecker and Stirling, 1878, who noted that 'red' striated muscle has a slower contrac• Dynamic and Static tion time than 'white' muscle fibres. Gamma Efferents This functional differentiation of mus• cle fibre types was supported by the Will \ \ i histochemical analysis carried out by extrafusal Fibres Kugelberg and Edstrom (1968) These researchers found that the motor units of slow 'red' fibres have a high content DNB = dynamic nuclear bag fibre SNB = static nuclear bag fibre, NC = nuclear chain fibre la = afferent from primary ending II = afferent from of oxidative enzymes. The oxidative secondary ending IN = interneuron umn = alpha motoneuron ymn = gamma motoneuron -—-= delineation of anterior horn of spinal cord enzymes are stored in the mitochon• Phastc stretch reflex quick stretch — DNB — la — phasic «mn -* efferent -* fast (witch extrafusal fibre This can be influenced by phasic mn dria, or 'power house', of a cell and discharge Tonic stretch reflex prolonged or slow stretch -+ SNB/NC - !a/ll - tonic are involved in the metabolic reaction omn -* efferent — stow twitch extrafusal (breakdown of ATP) to produce en• (phasic = dynamic tonic - static) ergy (Ganong 1973). As Edstrom (1973) wrote, this oxidative metabo• Figure 4: Diagrammatic representation of the phasic and tonic stretch reflexes

The Australian Journal of Physiotherapy Vol 29, No 5, October, 1983 163 The Neurophysiology of Tone

stretch to mtrafusal fibres of the mus• Therefore the primary endings on chemistry, ultrastructure, motor innervation, cle spindle. A small rapid stretch, DNB fibres would be particularly af• and regeneration of mammalian muscle spin• dles, Progress in Brain Research, 44, 67 87 imparted to the DNB fibres results in fected by dynamic gamma efferent Barker D, Emonet-Denand F, Harker DW, Jamie separation of the coils of the primary discharge Through these connections and Laporte Y (1976a), Distribution of fusi• motor axons to mtrafusal muscle fibres m cat ending, causing them to fire and gen• the dynamic gamma motoneuron in• tenuissimus spindles as determined by the erate an The rapidly fluences the sensitivity of the phasic glycogen-depletion method, Journal of Ph\- conducting la afferent fibre conducts monosynaptic stretch reflex. siologoy, 261, 49-69 Barr ML (1972), The Human Nervous System, the impulses to the ventral horn of Static gamma efferents may also 2nd edition, Hagerstown Md, Medical Books the spinal cord where there is a mon- innervate all mtrafusal fibres. The Department, Harper and Row, New Yoik osynaptic connection with phasic al• predominant effect of static gamma Bessou P, Emonet Denand F and Laporte Y (1965), Motor fibres innervating extrafusal and pha motoneurones. The impulses then stimulation has been found to be mtrafusal muscle fibres in the tat, Journal of pass along the efferents to the white contraction of SNB and NC fibres Physiology, ISO, 649-672 or fast twitch extrafusal muscle fibres This distorts primary and secondary Boyd IA (1956), The tenuissimus muscle of the cat, Journal of Physiology, 133, 35-36 and a contraction results. This is the endings, increasing their static or tonic Boyd IA (1957), The innervation of mammalian phasic monosynaptic stretch reflex and sensitivity, which can increase the sen• neuromuscular spindles, Journal of Physiol• is depicted diagrammaticaily in Figure ogy, 140, 14-15 sitivity of the tonic stretch reflex The Boyd IA (I960), The diameter and distribution 4. tonic discharge of alpha motoneurones of the nuclear bag and nuclear chain fibres in A prolonged or slow stretch pro• through the static gamma loops helps the muscle spindles of the cat, Journal of Physiology, 153, 23-24 duces the tonic stretch reflex. The to maintain normal muscle tone, par• Boyd, IA (1961), The motor innervation of effects of a slow stretch largely excite ticularly that of the anti-gravity pos• mammalian muscle spindles, Journal of Phys• the primary endmgs (static sensitivity) tural muscles. iology, 159, 7-9 Boyd IA, Gladden MH, McWilliam PN and and the secondary endings lying on Ward J (1975), 'Static' and 'dynamic' nuclear SNB and NC fibres. Impulses are bag fibres in isolated cat muscle spindles, Journal of Physiology, 250, 11-12 conducted along group la and group Conclusion Boyd IA (1976), The response of fast and slow II afferents to synapse in the spinal The muscle spindle plays a dominant nuclear bag fibres and nuclear chain fibres in cord. Here, part of the population of isolated cat muscle spindles, Quarterly Journal role in regulating muscle tone via the of Experimental Physiology, 61, 203-253 group II afferents reinforce la afferent phasic or tonic stretch reflexes These Boyd IA (1976a), The mechanical properties of activity, with both afferents making reflexes which provide the clay for dynamic nuclear bag fibres, static nuclear bag polysynaptic connections with tonic fibres and nuclear chain fibres in isolated cat normal tone, can be shaped or muscle spindles, Progress in Brain Research, alpha motoneurones. The tonic alpha moulded by peripheral, spmal or su- 44, 33-66 motoneuron discharges, and contrac• praspinal factors. Physiotherapists, Boyd IA, Gladden MH, McWilham PN and tion of 'red' slow twitch extrafusal Waid J (1977), Control of dynamic and static through the apphction of specific nuclear bag fibres and nuclear chain fibres by fibres results. treatment techniques, are able to alter gamma and beta axons in isolated cat muscle The second way in which muscle muscle spindle activity, thereby shap• spindle, Journal of Physiology, 265, 133-162 Brodal A (1962), — Anatomical As• spindles can be made to fire is via ing desired muscle tone and move• pects, Ada Neurohgica Scandinavia, Supple• stimulation of the gamma motoneu• ment ment 3, 38, 9-40 ron. Discharge of the gamma moto• Burie D, Lance JW (1973), Studies of the reflex effects of primary and secondary spindle end• neuron causes contraction of the m- ings in spasticity, m Desmedt JE (ed ), New trafusal fibres, subsequent distortion Developments m Electromyography and Clin• ical Neurophysiology, 3, 475-495, Karger, of the sensory (primary and secondary) Basel endings and propagation of impulses Chapman C, Michalski, Siguin (1979), The effects along the group la and group II of cold-induced muscle spindle secondary ac• tivity on monosynaptic and stretch reflexes in afferents to the spinal cord where References the decerebrate cat, Canadian Journal Physi• synapses are made with the alpha Ada! MN and Barker D {1965), Intramuscular ology and Pharmacology, 57, 606-14 motoneurones. In this way, the gamma branching of fusimotor fibres, Journal of Cooper, S, Daniel PM and WhiUendge D (1955), Physiology, 177, 288-299 Muscle spindles and their sensory endings in motoneuron can influence alpha mo• Barker D (1962), The structure and distribution the extrinsic eye muscles The physiology and toneuron dicharge and this is what is of muscle receptors, in Barker D (ed ), Sym• anatomy of these receptou and of their con• often referred to as "driving the alpha posium on Muscle Receptors 227-240, Hong nexions with the brain stem, Brain, 78, 564- Kong University Press, Hong Kong 583 motoneuron through the gamma Barker D and Gidumal JL (1961), The mor• Cooper S and Daniel PM (1963), Muscle spindles loop' phology of mtrafusal muscle fibres in the cat, in man, their morphology in the lumbrical and Journal of Physiology, 154, 513-528 the deep muscles of the neck, Biam, 86, 563 Although dynamic gamma efferents Barker D, Stacey MJ and Ada! 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164 The Australian Journal of Physiotherapy Vol 29, No 5, October, 1983 The Neurophysiology of Tone

Eccles JC, Eccles RM, Iggo A and Lundberg A Kanda K, Rymer WZ (1977), An estimate of the Matthews PBC (1968), Receptors in muscle, (1960), Electrophysiological studies on gamma secondary spindle receptor afferent contribu• Physiotherapy, 54, 204 motoneurones, Acta Physiologica Scandinavia, tion to the stretch reflex in extensor muscles Matthews PBC (1969), Evidence that the second• 50, 32-40 of the decerebrate cat, Journal of Physiology ary as well as the primary endings of the Edstrom L (1973), Relation between spasticity (London), 264, 63-87 muscle spindles may be responsible for the and muscle atrophy pattern tn upper motor Katz B (1946), The efferent regulations of the tonic stretch reflex of the decerebrate cat, neurone lesions, Scandinavian Journal of Re• muscle spindle in the frog, Journal of Exper• Journal of Physiology, 204, 365-393. habilitative , 5, 170-171 imental Biology, 26, 201-217 Matthews PBC (1973), The advances of the last Eldred E and Tokizane T (1955), Two patterns Kirkwood PA and Sears TA (1974), Monosynap- decade of animal experimentation upon muscle of afferent discharge from muscle spindles, tic excitation of motoneurones from muscle spindles, in Desmedt JE (ed ), New Develop• American Journal of Physiology, 183, 612 spindle secondary endings of intercostal and ments in Electromyography and Clinical Neu• Eldred E (1965), The dual sensory role of muscle triceps surae muscles in the cat, Journal of rophysiology, 3, 95-125, Karger, Basel. spindles, Journal of the American Physical Physiology (London), 245, 64-66. 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