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The Neuropnysiology of Tone: The Role of the

Muscle Spindle and the Stretch Reflex

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

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 tendon organ synapses with
obtaining at any one moment between afferents into the spinal cord. 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
tendons, muscles and the connective reflex muscle contraction. (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 motor unit activity. whole muscle and this led Matthews
As motor unit activity is influenced The Golgi Tendon Organ (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
grey matter 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.
Tendon <+- -<<h
To Agonist
Organ Intrafusai Fibres
In 1956, Boyd identified two to
three large intrafusai fibres and two
-<o- <o- To Antagonist
to five small intrafusai fibres in the
tenuissimuss muscle of the cat. Cooper
and Daniel (1963) studied human mus-
^ inhibitory mterneurone cle spindles and also identified two
{ facihtatory mterneurone distinct types of intrafusai fibres based
on the distribution of their central
crmn alpha motor neuron
nuclei. The fibres lose their stnations
and appear to be non-contractile and
Figure 1: Diagrammatic representation of autogenetic inhibition
less viscous in the nucleated region
(Eldred 1965). These fibres are known
as nuclear bag and nuclear chain
tinuous part in the central regulation fibres), together with afferent and
of muscle tone, rather than simply efferent nerve endings, enclosed in a Nuclear Bag Fibres
being reserved for use in emergencies. connective tissue capsule (Matthews Matthews (1973) described nuclear
The reflex connections of the Golgi 1973). This capsule encloses the intra- bag fibres as having a cluster or bag
tendon organ with the Alpha motor capsular space which extends about 1 of nuclei lying two to three abreast at
neurones of the agonist (autogenetic mm on either side of the equator in the spindle equator, with a few nuclei
inhibition) and the functions ascribed living spindles (Boyd 1976). The mtra- lying at the periphery of the fibre.
to this receptor by Ganong (1973) capsular fluid within this space has a According to Eldred (1965), some of
(protective role) and Matthews (1973) mucopolysaccharide constituent and is these fibres pass beyond the connective
(contraction receptor) indicate that probably viscous (Eldred 1965). It is tissue capsule as 'percapsular' fibres
this receptor could not be responsible thought to insulate nerve endings from and are larger in cross section than
for the reflex muscle contraction ob- local mechanical disturbances (Mat- the intracapsular fibres.
served by Liddell and Sherrington thews 1973). Two types of nuclear bag fibres,
(1924). Rather, the receptor responsi- According to Eldred (1965), the 'bag 1' and 'bag 2' fibres have been
ble for the contraction of a muscle in muscle spindle lies in an interfascicular distinguished by Ovalle and Smith
response to stretch is now known to cleft parallel to the extrafusal fibres (1972) on the basis of their ATP ase
be the muscle spindle. and is usually near an intramuscular staining reactions Bag 1 fibres have
nerve and artery. This 'in parallel' low staining reactions for ATP ase,
The Muscle Spindle arrangment means that the muscle whereas bag 2 fibres have medium to
Eldred (1965) wrote that muscle spindle will be stretched at a similar high staining reactions. ATP ase is
spindles were first noted in growing rate and to a similar degree as the the enzyme which hydrolyses ATP
muscles as small fibres with central extrafusal fibres. (adenosine-tri-phosphate), a high en-
nuclei. They resembled the fibres Brodal (1962) reviewed the work of ergy storing compound, to give ADP
found in developing muscle fibres and researchers in the field of muscle (adenosine-di-phosphate) free phos-
were therefore thought to be sources spindle anatomy and physiology and phate and energy (Ganong 1973).
of myogenesis and were termed 'mus- noted that muscle spindles are located The difference in the ATP ase stain-
cle buds'. Eldred (1965) continued that in all the muscles of locomotion, in ing reactions indicates a difference in
in 1884 Mays suggested that the muscle the laryngeal muscles, muscles of mas- the energy requirements of the bag 1
spindle might be a sensory organ, a tication, the tongue, and in the extrin- and bag 2 fibres This is further
view supported by Cajal in 1888. sic ocular muscles. Muscles used in reflected in the number of mitochon-
Ruffini (1897) claimed that at least delicate movements such as the mus- dria within each fibre. The mitochon-
two types of sensory endings were cles of the hand have a greater density dria are often referred to as the 'power
discernible in mammalian spindles. of muscle spindles than do muscles generating units' of a cell because it
The muscle spindle is, in fact, a used in coarser movements, such as is here that the oxidative enzymes
bundle of up to ten small specialized the muscles of the trunk. The muscle involved in the reactions providing
striated muscle fibres (intrafusai spindles of any of these muscles have energy for the cell are found (Ganong

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
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 myofilaments, 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
myosin, a muscle protein When of nuclear bag fibres by studying the 1973).) This suggests that the energy
myosin is combined with actin, 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 axon 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 endomysium.
(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 spinocerebellar tract
fusal fibre, the structure of the ending, at low tensions would go unnoticed. which activates the cerebellum 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

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

The Neurophysiology of Tone

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 synapse 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
Supraspinal Eldred (1965) explained that the
secondary endings are continuous with
Spsnal Level the myehnated group II afferent axons
which have a diameter of 4-12^. As
-<- -<0-
amn To Antagonist
the group II fibres have a smaller
diameter than the group la afferents,
their nerve conduction velocity is
r~<4 (0- To Synergtst or
slower (Erlanger and Gasser 1924).

Agonist (a) Location and Sensitivity to Stretch

Primary Endtng
h To Agonist
Boyd (1957) found that secondary
endings are located on nuclear chain
and fa Afferent fibres, lying on either side of the
^ inhibitory interneuron primary ending; that is, lying juxta-
^ facihtatory mterneuron equatorially. Hunt's (1954) experi-
amn alpha motor neuron 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 nervous system 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

160 The Australian Journal of Physiotherapy Vo! 29, No 5, October, 1983

The Neurophysiology of Tone

(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: Motor Control 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

The Australian Journal of Physiotherapy Vol 29, No 5, October, 1983 161

The Neurophysioiogy of Tone

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 'p 2 ' 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 i n d i v i d u a l m o t o r 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;
fibres and are, according to Matthews Emonet-Denand, Jamie and Laporte
thews (1973), the secondary endings
(1973), controlled exclusively by static 1975; and Boyd, Gladden, McWilliam
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.
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
is in keeping with the faster dynamic f

muscle contraction resulting fiom / Influence

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
motoneurones in the maintenance of
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
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
(phasic = dynamic tonic - static)
(breakdown of ATP) to produce en-
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,
and regeneration of mammalian muscle spin-
cle spindle. A small rapid stretch, DNB fibres would be particularly af- 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 action potential 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 Boyd IA (1956), The tenuissimus muscle of the
This distorts primary and secondary 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-
ogy, 140, 14-15
is depicted diagrammaticaily in Figure 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-
tural muscles. iology, 159, 7-9
the primary endmgs (static sensitivity) 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
Waid J (1977), Control of dynamic and static
tion of 'red' slow twitch extrafusal 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 spindle, Journal of Physiology, 265, 133-162
muscle spindle activity, thereby shap- Brodal A (1962), Spasticity 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
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The Australian Journal of Physiotherapy Vol. 29, No 5, October, 1983 165