myotatic reflexes in sympathectomised muscle

Myotatic Reflexes in Sympathectomised MuscleAuthor(s): Gilbert PhillipsSource: Proceedings of the Royal Society of London. Series B, Containing Papers of aBiological Character, Vol. 110, No. 768 (May 2, 1932), pp. 412-430Published by: The Royal SocietyStable URL: http://www.jstor.org/stable/81652 .

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412 G. Phillips.

FIG. 2.-Skin of dog No. 2. Several hair follicles are surrounded by infiltrations of macrophages. The intervening dermis is normal. (Magn. 80 X.) Infection rate in P. perniciosus, 65 - 4 per cent.

FIG. 3.-Skin of dog No. 1. Infiltration round hair follicles and sebaceous glands. Small areas of infiltration in dermis. (Magn. 80 X.) Infection rate in P. perniciosus at time skin was taken for section, 90 per cent.

PLATE 20.

FIG. 1.-Infected macrophages round a sebaceous gland. (Magn. 820 X.) FIG. 2.-Infected macrophages in the neighbourhood of a hair follicle. (Magn. 820 X.) FIG. 3.-Infected macrophages in the normal dermis. (Magn. 820 X.) FIG. 4.-Single large infected macrophage in normal dermis. (Magn. 820 X.) Note

absence of tissue reaction in figs. 3-4.

6I2 . 833: 6I2 . 748. o89. 87

Myotatic Reflexes in Sympathectomised Muscle.

By GILBERT PHILLIPS, M.B., B.S., M.Sc., Liston Wilson Fellow (Univ. Sydney), Fellow of the Rockefeller Foundation.

(Cormmunicated by Sir Charles Sherrington, F.R.S.-Received January 21, 1932.)

(From the Physiological Laboratory, Oxford.)

[PLATES 21-23.]

Introduction.

As a result of their experiments on normal, spinal and decerebrate animals

Hunter and Royle (1924) concluded that the post-ganglionic fibres of the sympathetic nervous system constituted the efferent limb of the reflex arc

subserving postural contraction in skeletal muscle. In a recent article (1931)

the present author described a series of experiments on decerebrate cats in

which Royle's observation of diminished resistance to passive flexion in a

sympathectomised " decerebrate " extensor muscle was confirmed, but the

hypothesis that this was due to a " tonic " nervous influence of sympathetic

axones on skeletal muscle fibres was denied. This denial was based on the

fact that postural contraction was modified but not abolished by sympathectomy,

and that the operation actually enhanced such proprioceptive reflexes as the

shortening reaction and the crossed extensor reflex of Philippson (1905).

Finally it was suggested that the diminished resistance of the extended " de-

cerebrate " limb to passive flexion and the enhancement of those proprioceptive



Myotatic Reflexes in Sympathectomised Muscle. 413

reflexes which could be elicited by stretching the sympathectomised muscle

were produced by a disturbance of the excitability of its proprioceptive end- organs.

Denny-Brown (1928), after studying postural reflexes, :has stated that the

sympathetic nervous system is not essential to the stretch reflex, but he further stated that he was unable to discover any effect on general posture by excision of the sympathetic.

The present author has now repeated his own previous wo:rk and has examined the myotatic reflexes of single sympathectomised muscles by means of Sher- rington's isometric myograph and fall-table.

The naked eye observation of single muscles during the dissection of the limbs of decerebrate cats has thrown further light on the difference in the behaviour of the normal and the sympathectomised muscle. Stretching the tendon of a " decerebrate " soleus muscle, within 1 or 2 hours after removal of its sympathetic innervation, produces a strong postural contraction which closely resembles the response elicited by the same stimulus from the normal muscle. If the stretching force be moderate the contraction appears to be equally well maintained in both muscles; if, however, the applied tension

be increased, the resistance of the sympathectomised muscle yields first, and the whole muscle extends under the influence of the lengthening reaction.

This liability to undergo reflex lengthening is increased as the interval of time following sympathectomy increases up to a period of at least 3 weeks. In the " chronically sympathectomised " muscle (from 10 to 80 days following operation) the gradual application of tension appears to produce a series of " fractional " lengthening reactions, in which slight early resistance and partial relaxation follow one another in rotation, until considerable tension is developed by passive stretch of the muscle elements. If the muscle is stretched sharply, the response is not unlike that of a flexor muscle; there is at first a strong " pluck " reflex, followed by a lengthening reaction, and at this new length the muscle may exhibit a weak postural contraction.

Sympathectomised muscle displays a marked tendency to exhibit clonic

movements, both in acute and chronic preparations. Clonus, usually a

prominent feature of intercollicular decerebrate preparations manifesting good rigidity, is profoundly influenced by tonic vestibular and neck reflexes, so that for comparative purposes a symmetrical disposition of the animal is essential. Under such conditions, one may say that the sympathectomised muscle is always, as it were, on the verge of substituting clonus for postural contraction. Any unevenness in the rate of stretch is sufficient to brirLg about rapid clonic



414 G. Phillips.

movements, of very slight tension, in the sympathectomised mauscle. The chief "clinical" differences to be observed, between clonus on the normal and sympathectomised sides, are that, in the latter, the rate appears to be more

rapid and the clonic movements occur over a wider range of tension. In the normal mruscle, clonus, which occurs over an optimal range of tension, may be arrested by the application of further stretch to the tendon. In the sympathectomised muscle such further stretch may arrest clonus for several beats, during which time the muscle may be felt to lengthen, with the subsequent resumption of clonus at this new length. The profound influence of the tonic neck and vestibular reflexes, in producing a subliminal excitatory state at the central motoneurone pool, is well demonstrated when, with the head and neck in the "C maximal" position, the freely dissected sympathectomised muscle, lying slack on its surrounding muscular bed, may be seen to be in clonus. Such atonic clonic movements, which have not been observed in the normal muscle, can only be produced by the centripetal excitation, resultant on sympathectomy coinciding with the subliminal excitatory state already existent in the motoneurone pool. That this is so is shown by cessation of clonus where the head and neck are moved to a less maximal position.

Further evidence, of peripheral excitation summing with a subliminal central excitatory state, has been seen in several decerebrate cats in which rigidity was not marked. When these animals were disposed symmetrically with the head and neck in the " maximal " position the sympathectomised limb might be seen to exhibit a partially extended attitude while the normal limb remained flexed. This asymmetry, which has been noted before (Phillips, 1931), depends upon a stronger postural contraction in sympathectomrised muscles, produced almost certainly by increased proprioceptive excitation; it being assumed that a constant inequality in vestibular or cutaneous influence is most unlikely over a series of animals.

From clinical evidence it may be said that sympathectomised muscle retains in great degree its power to respond to a stretching force by contracting, loses in great degree its ability to maintain a postural contraction, and in place of the latter displays a tendency to replace tonus by clonus. The subsequent myographic analysis substantiates and amplifies this s-ummary statement.

Technique.

A double mirror type myograph as described by Sherrington (1928) and Eccles and Sherrington (1929) has been used in making simultaneous records from two corresponding muscles. The twin torsion wires of this myograph




were either 94/1000 or 64/1000 inch in diameter. The former pair were used for examining stretch reflexes, the latter for muscle jerks ancd records of clonus. Both pairs of wires were calibrated and proved to record eq[ual deflections for equal loads. A modification was made in the original designL of the myograph, a third mirror being attached just below and between the twin torsion wire mirrors. This could be rotated into a suiitable position before attaching the muscles to the myograph and then fixed by a small binding screw so that it recorded a base line of zero tension to both torsion wires. A-a optical recording system was used, in which the image of an illuminated slit was reflected by the three myograph mirrors on to a falling plate camera.

Graded stretch stimulation was provided by means of a Sherrington pattern fall-table (1924).

The sympathetic chains have been removed from 35 cats through a midline incision in the anterior abdominal wall, the whole extent of each chain being excised from the crus of the diaphragm above, down to and including the second sacral ganglion below. In 25 animals the left chain was removed, in 8 the right chain, and in 2 cats both chains were excised. Twelve of these cats were decerebrated and examined immediately after the sympathectomy, while 23 were allowed to recover from the operation and were decerebrated and examined from 10 to 80 days later. In the cat the midline operation offers the best approach to the abdominal sympathetic chains, since it permits a clear view of both of them. One chain may be removed en bloc by caref ul blunt dissection wit-hout disturbing the relations of its fellow of the opposite side. Post-mortem examination always confirmed the integrity of the un- disturbed chain on the control side. Protected by the sheath of extraperitoneal fat in which it lies, it was never seen to be involved in the peritoneal thickening and mild fibrosis succeeding the operation.

The soleus muscles of decerebrate cats have been shown to be the seat of a strong stretch reflex (Denny-Brown, 1928); their fibres are relatively parallel and their almost linear origin permits a widespread separation of the nmuscle belly from the surrounding soft tissues. By virtue of these qualities they were selected as presenting a suitable bilateral preparation for the comparative study of postural reflexes in homologous muscles. They were prepared for the myograph by free dissection of the muscular bellies from the surrounding soft tissues. At the site of their insertions a small piece of bone was chipped off the calcaneum and left attached to the tendon. All other muscles in both hind limbs were paralysed by motor nerve section, and the cutaneous nerves were divided according to the technique described by Sherrington (1909). The decerebrate animal was placed prone on the fall-table with the trunk directed at right angles away from the myograph and supported on each side by warm bottles. The head was extenided and maintained erect in the midline by attaching to an upright stand a loop of the silk used for sut-uring



416 G. Phillips.

the scalp wound. The fore limbs were extended side by side on the table surface. The hind limbs were fixed to the fall-table in the same vertical plane by means of drills inserted transversely through the upper and lower ends of the tibiwe. With the origins of the soleus muscles fixed in this manner their respective tendons were attached to the horizontal tension bars of the torsion wires by means of hooks of adjustable length. These hooks, constructed like small union screws, an insulating fibre cylinder forming the union, permitted a separate adjustment of the length or tension in each muscle. When the table was allowed to fall through a known distance the two soleus muscles linking it to the rigid myograph were submitted to the same stretching force.

The electric responses were led away from each muscle by silver chloride-coated electrodes to a double string galvanometer. Shadows of the two galvanometer strings were projected on to the slit of the falling-plate camera. The silver chloride electrodes were inserted in corresponding regions of the two muscles approximately to the same depth and at the same distance apart. The tension in the galvanometer strings was adjusted before each plate- record, so that a potential difference of 1 millivolt produced a deflection of 15 mm. in each string.

Myotatic Reflexes.

The quality of plasticity exhibited by " decerebrate " muscle demands a low initial tension in making simultaneous comparative records of stretch reflexes in two muscles. The term " plasticity," originally applied by Sher- rington (1909), expresses the ability of the muscle to present the same tension at different lengths. This quality, then, when two " decerebrate " muscles are submitted to the same tension, may result in unequal length; an asymmetry which carries in its train an unequal development of tension on the application of further stretch. It is important therefore to ensure the same initial length in the two muscles before they are stretched. This was accomplished as follows: The two union-screw hooks were suspended on their respective tension bars and the three myograph mirrors rotated so that the beams of light reflected by them were focussed at one point on the camera slit, this point being that of zero tension in both torsion wires. The fall-table was then raised and each soleus tendon impaled on its hook, both muscles being quite slack. The hooks were then shortened separately, taking up the slack in the muscles until tlhe first minimal deviation of the mirror beams, away from the base line of zero, could be observed. Under such conditions each muscle was subjected to an initial tension of less than 5 grams, and, as can be seen in the records, the galvanometer strings were " silent," or exhibited activity in only one or less frequently two muscle fibre units, before the onset of the table fall. This bilateral minimal posture has been taken as the starting point for the comparison of the responses of the normal and sympathectomised muscles to stretch.

Control myograms in five animals, either with both sympathetic chains



Myotcttic Reflexes in Sympathectomised Muscle. 417

intact or both excised, have shown, in records from both soleus muscles, the

simultaneous development of tension at the same rate with the achievement of

approximately the same final plateau tension, provided that the amount of

stretch was small, the rate of stretch constant and the initial tension low. If

these conditions were satisfied, the muscles under a stretch of 3 mm. carried

out at an even rate presented a strong myotatic reflex over 90 per cent. of which

was constituted by active contraction. If the amount of stretch was increased

beyond 6 mm., the passive tension produced by stretch of muscle elements

claimed a much larger percentage of the total tension, fig. 10, Plate 22. The

electric responses set up by the table fall in the soleus muscles of normal or

bilaterally sympathectomised cats always appear within 5 s:igma of each other, figs. l and 2, Plate 21. The latent periods of the myotaticreflexes in the muscles

of bilaterally similar preparations can be said, therefore, to vary under the

present technique by less than 5 sigma. Myograms taken from decerebrate cats, in which the sympathetic chain has

been removed on one side, display characteristic differences on the two sides, both in the mechanical and the electrical records. It is w-orthy of note that

these differences were not due to asymmetrical decerebration, since they were

constantly present in 35 animals. Intercollicular decerebration bv unilateral subtemporal craniotomy, the operation performed in each case, has beeil shown

by post-mortem examination to permit a macroscopically symmetrical brain- stem section. That the changes were not produced by centripetal impulses streaming in from skin wounds has been proved by dusting these with an anaesthetic powder.

The sympathectomised muscle attains for the same stretch a greater myotatic tension, fig. 3A, Plate 21, and its mechanical record arises more'sharply from the base line, fig. 3, Plate 21. In an acutely sympathectomised muscle a final plateau of moderate tension is fairly well maintained in some cases. This contrasts with the behaviour of chronically sympathectomised muscle, which does not maintain even a moderate plateau tension, the mechanical record

falling, in contrast with the normal side, to a lower level, fig. 5, Plate 22, on the one hand, or, on the other, passing into clonus, fig. 8, Plate 22. In chronic

preparations the tension ascent from the base line follows a series of hump-like contractions, fig. 5, contrasting with the tolerably smooth ascent of the tension curve of the normal muscle. This uneven rise is due to synchronous contraction in several muscle fibre units, a form of activity which, as will be shown later, is reflected in the galvanometer record.

The electric responses at once point to a much shorter latent period of the



418 G. Phillips.

stretch reflex on the sympathectomised side. In fig. 4, Plate 21, where, in the minimal posture described above, a single unit is firing in each string before the application of stretch, the electric responses commence some 50 sigma earlier on the sympathectomised side after the onset of the table fall. This earlier response, also seen in fig. 3A, Plate 21, may be taken as an expression of the fact that the centripetal impulses flowing in from the two muscles produce a central excitatory state which first becomes liminal in the motoneurone pool of the sympathectomised muscle. This earlier achievement of centrifugal firing, under identical external conditions of peripheral stimulation, may be due either to the activity of more proprioceptive end organs, or to the enhanced activity of the same number, or to both factors occurring together. In normal muscle, both during the application of stretch and during the maintenance of postural contraction, unless it be of that slight order produced by the activity of but a few units, there is to be found a characteristic and complete asynchronism of firing (Fulton and Liddell, 1925), seen in the electrical record as a restless series of small deflections. This asynchronism, produced by the application of stretch at an even rate, is responsible for the steady rise of the mechanical record. In sympathectomised muscle, both during the application of stretch at an even rate and following the achievement of the final plateaui, there can be seen to be many short " silent periods " in the activity of the galvanometer string. They produce the uneven ascent in the mechanical record, where they may occur simultaneously with an increase in mechanical tension, the latter representing the after-action of the preceding contraction shown by the large compound action currents, fig. 2, Plate 21. These " silent periods "

therefore do not represent the lengthening reaction, although they must be due to the temporary predominance of proprioceptive inhibition, producing, in conflict with proprioceptive excitation, a transient central inhibitory state in the motoneurone pool. The descent of the plateau tension, the contraction being isometric and associated with short periods of subliminal central excitation, is explained by the fact that the falling tide of central excitation at the onset of each " silent period " is no longer reinforced by the rising tide of peripheral excitation, associated with increasing stretch during the table fall.

These " silent periods " are no doubt the basis of the clinical plhenomena in chronic sympathectomised muscle which earlier in this paper have been termed " fractional " lengthening reactions. They are present, but less obvious, in acute sympathectomised muscle, fig. 3A, Plate 21. That the influence of sympathectomy has not been to bring proprioceptive inhibition alone into a prepotent condition is shown both by the greater tension achieved by sympa-




thectomised muscle during stretch and by the characters of the action currents produced by such contraction.

The electric responses from sympathectomised muscle always include large compound waves diphasic in type which are not characteristic accompaniments of evenly applied stretch to normal muscle, fig. 3A, Plate 21. These waves are evidence of the synchronous or almost synchronons activity of several muscle fibre units, that is of two or more cells of the motoneurone pool. This is^ interpreted as being due to the simultaneous activity of several proprioceptive end organs in their firing into the motoneurone pool which is a parallel with the mechanism suggested to be responsible for the shorter lat,ent period of the

stretch reflex in sympathectomised muscle. It is the simultaneous activity of several centripetal afferents which is emphasised rather than the general intensification of their individual activity.

Denny-Brown has demonstrated the profound influence of proprioceptive inhibition on the motoneurone pool not only of the excited muscle but also of other muscles (1928).

The intensity of such inhibition is largely conditioned by the extensity of synchronous firing in muscle fibre units. In normal muscle wvith the galvanometer string record as an index, proprioceptive inhibition achieves a maximum in the synchronous contraction type, the muscle jerk, where the length of the " silent period " is proportional to the height of the jerk contraction and is seen to be at a minimum in the completely asynchronous firing of steady maintained postural contraction. Sympathectomised muscle is believed to achieve an intermediate position of incomplete synchronisation in which asynchronous characteristics such as steady posture are in great degree lost, while, as will be shown later, synchronous activity such as clonus and the muscle jerk are in great degree enhanced.

The thesis set down above to explain the fall of postural tension shown by the decline of the mechanical record following stretch suggests in the light of the alternating central excitation and inhibition manifested in the electric responses from sympathectomised muscle that the rate of stretch may be a critical factor in determining the maximum tension achieved by the resultant myotatic contraction. That such is not the case in normal muscle may be seen from the original records published by Liddell and Sherrington (1924) where a slow stretch produced an even greater maximum tension than the same stretch carried out at a very fast rate.

The records they publish, however, were produced by stretches of 8 mm. with a resultant passive tension of more than 35 per cent. of the total. With



420 G. Phillips.

this factor eliminated it may be seen that the same stretch applied either slowly or rapidly to normal " decerebrate " muscle elicits within limits the same maximal tension. On the other hand, this does not occur with sympathectomised muscle, which under the slow stretch fails to achieve as great a tension as under the fast, figs. 12 and 13, Plate 23. There is therefore a critical rate of stretch at which the normal and sympathectomised muscle should achieve the same maximum tension, a rate which is very closely represented in fig. 5, Plate 22. With rates faster than this the sympathectomised muscle contraction is greater than the normal myotatic contraction and with slower rates it is less.

All these foregoing observations are regarded as an expression of the alternating synchronous activity and " silence " in the galvanometer string record from the sympathectomised muscle. They are considered to be based upon the quantitative value of the rising tide of peripheral excitation produced by graded rates of stretch occurring during the critical " silent period " in the string record. If this excitation be small there is but slight reinforcement of the mechanical tension, if it be large the contraction is strongly reinforced. The absence of such " silent periods " with complete asynchronous firing in the normal muscle removes this factor determining the maximum tension to be achieved.

That there is little or no change in the activity of proprioceptive end organs of low threshold following sympathectomy is proved by examining the rate of firing of single muscle fibre units under minimal conditions of applied tension. It might be expected that if the excitability of low threshold receptors was increased by sympathectomy, the rate of firing of single muscle fibre units would be faster in the sympathectomised muscle than in the normal when the same minimal stretch was applied to both museles. To examine this the decerebrate cat was attached and suspended in the prone position to a horizontal steel bar by means of vertebral clamps. With the animal's body in a symmetrical position the freely dissected soleus muscles depended from their bony origins alone. The muscle electrodes were inserted as before and corre- spondingly small weights were attached to each tendon. When a 2 gram weight was suspended from each soleus it was found in many instances that a single unit was caused to fire in each muscle, fig. 6, Plate 22. Both on the normal and sympathectomised sides the rate of firing was found to correspond almost exactly and to vary from 9 to 11 per second. Such minlimal stretch was seen therefore from the nature of the centrifugal firing to produce identical streams of centripetal excitation from each muscle. If, however, the 2 grams were




substituted on each side by a 10 gram weight a great difference in the electric responses was at once evident, fig. 7, Plate 22. The added stretch was usually only sufficient to bring into action two or three more units. Owing to asynchronous firing each unit was capable, by analysis, of isolation from its fellows. On the sympathectomised side, however, the same stimulus produced firing in too many units to permit their number to be determined. The string record was characterised by the presence of large compound waves, diphasic in type, alternating with periods of " silence," indicating a state of partial synchronism bordering on clonus. It seems justifiable to conclude from this latter observation, in the light of the local nature of stretch excitation, that a greater number of proprioceptive end organs were in simultaneous activity in the sympathectomised muscle and were prolucing an almost svnchronous firing in several motor nerve cells. The influence of sympathectomy was, therefore, to produce a greater concentration of tension receptor activity at low threshold by activating end organs, which in. the normal muscle could only be brought irtto play by the application of further stretch.

Muscle Jerks and Clonus.

The soleus jerks have been compared by means of an electromagnetically released myograph. This instrument, fig. 1, for whose construction I am

FIG. 1.-Diagram of the electromagnetically released triple mirror myograph used for recording soleus jerks.

indebted to Mr. O'Neill of this laboratory, consists essentially of the three mirror myograph outlined above with torsion -wires of 64/1000 inch diameter. Small brass blocks are mounted on the ends of the horizontal tension bars of the torsion wires and through these blocks iron screws are inserted with their points upward and their flat circular heads downward. Mounted below the solid brass base of the myograph, a stage projects carrying two single pole



422 G. Phillips.

electromagnets, the soft iron core of each of which is so placed that it lies immediately below the circular head of one of the iron screws. When a current at a potential of 6 volts is passed in series through the two electromagnets the screws are pulled down on to the soft iron cores, and with the magnification provided by the optical recording system a considerable deflection of the mirror beams is produced at the slit of the camera. The height of each iron screw is then adjusted so that the extent of this deflection is the same for the two beams. At the instant of breaking the circuit in the magnet coils the screws are released from the iron cores and the unbalanced torque in the torsion wires produces an iimuediate return of the mirror beams to and beyond the zero base line about which they vibrate with the natural period of the wires before coming to rest.

This instrument provides a means of applying the same instantaneous stretch to two muscles, thereby producing comparable records of muscle jerks. To examine these the decerebrate animal was arranged in the position described for the myotatic reflex with the two soleus muscles attached to the myograph under identical conditions of minimal stretch. The fall table was then lowered just enough to cause a 5 mm. deflection of the torsion-wire beams away from the zero base line at the camera slit. As the screws of the electromagnetic release were so adjusted that on closing the circuit equal deflections of at least 40 mm. were produced in each beam the two soleus muscles were then subjected to identical conditions of mininal stretch posture. On breaking the circuit both muscles were submitted to the same slight instantaneous stretch with the production of typical muscle-jerks. Control observations using two normal " decerebrate " muscles showed corresponding jerks in both, as judged by the amount of tension developed, the characters of the action current, and the length of the " silent period." Sympathectomised muscle, however, always presented under these conditions a jerk of greater tension, accompanied by a larger action current wave and a longer " silent period " than in the normal muscle, figs. 8 and 11, Plate 22. Following the jerk sympathectomised muscle often relapsed into a condition of incomplete clonus, fig. 8, Plate 22. Soleus jerks produced by tapping the table with a rubber covered rod always elicited a contraction of greater magnitude on the sympathectomised side, fig. 9, Plate 22. To the isotonic nature of the contraction and the weight of the leg is due the probable explanation of the failure to detect a larger amplitude of the knee jerk in the sympathectomised limb when the decerebrate animal is examined clinically.

It has been found difficult to obtain bilateral records of clonic movements due no doubt to interference in the corresponding " half-centres " of the cord.




The records which have been obtained, however, show in accordance with the clinical observations made above that in sympathectomised muscle clonus is more prone to occur, occurs at a much faster rate and may be manifested at all postural tensions of which the muscle is capable, it being remembered that steady posture of other than moderate tension is not3 seen in sympathectomised muscle. Fig. 14, Plate 23, shows a record of bilateral clonus, in -which the low tension and rapid clonic rate has produced a wavering mechanical record rather than a true clonic record. From the electrical records, however, -it may be seen that while the normal muscle beats at a rate of 15 per second, with definite synchronous action current waves alternatinlg with periods of -complete or almost complete string " silence," the sympathectomised muscle on the other hand is beating so quickly that the rate is difficult to determine, the action current waves are very small and are so close together that the "; silent periods " are almost abolished. The rate of clonus depends funda- mentally on the brevity of the " silent periods." The concentration of receptors at low threshold provides a rapidly rising tide of pe'ripheral excitation early in the onset of clonic relaxation, determined by the central inhibitory state, which is itself produced by the preceding synchronous firing. It is believed that sympathectomy influences clonus in this way in that the synchronous firing of receptors at low threshold sets up a wave of centripetal impulses which abolishes the " silent period " immediately after its onset, and replaces it by a weak central excitatory state in a few cells of the motoneurone pool. In this way there is produced centrally a rapid alternation of just supra-liminal and just sub-liminal excitation which is manifested peri- pherally as a rapid clonus of low tension.

Whenever the proprioceptive end organs of sympathectomised muscle are -used to excite contraction either in the muscle itself or in other muscles the characters of such contraction, as judged by the galvanometer string record, are those that have already been noted. Traction on the tendon of one soleus sufficiently strong to produce a lengthening reaction in it excites contraction in the opposite soleus. This is a similar reflex to that described by Philippson ((1905) for the quadriceps femoris. A contraction of greater tension is produced in the reacting soleus when the sympathectomised muscle is used to 'excite it than when the normal muscle is employed, fig. 16, Plate 23. And yet it may be noted that soleus contraction produced by faradic stimulation of a contralateral muscle nerve is equal in both the normal and sympathectomised muscles.

It is the inclusion of the receptor end organs in the reflex arc that produces the



424 G. Phillips.

observed changes in contraction tension following sympathectomy. In this Philippson type-reflex the nature of the centrifugal excitation sampled by the reacting soleus may be observed in the galvanometer string record. When the sympathectomised soleus is used as the exciting muscle the string record from the reacting muscle displays the characteristic large compound waves and short periods of " string silence " described before. With the normal soleus as the exciting muscle the string record displays completely asynchronous activity, with little or no sign of transient central inhibitory state, fig. 16.

This is regarded as evidence of concentration of receptor activity at low threshold in svmpathectomised muscle.

Discussion.

It is felt that the analysis of changes of receptor threshold in sympathectomised muscle presents a formidable problem, but nevertheless it is believed that a satisfactory working hypothesis may be constructed from the foregoing evidence. It is at the same time important to state, in agreement with Denny-Brown, that there is no evidence that the sympathetic innervation to skeletal muscle, plays any qualitative part in postural reactions, and that changes in proprioceptive reflex action (Royle, 1924) which have been thought to do so may be explained on a basis other than the sympathetic motor innervation of muscle fibres.

A significant observation is the progressive change in reflex action following sympathectomy; the loss of steady postural contraction and the tendency to display clonic movements becoming most prominent some weeks after the operation. Without predicting the results of another investigation which is, being prosecuted at the present time it may be said that there is some evidelice pointing to a considerable change in the vascular pattern of chronic sympathectomised muscle.

Analysis of the lengthening reactions in normal and sympathectomised nuscle throws some light on the behaviour of proprioceptive end organs under graded threshold of stretch. This reaction, originally described by Sherrington, is that " melting " of resistance and passive extension of a " decerebrate" muscle when an increasing tension is applied to its tendon.

It may be said to constitute the clinical basis for the estimation of so-called "tonus " in skeletal muscle, and, as has been stated above, is produced at a lower threshold of applied tension in sympathectomised muscle. It is a reflex action in so far that it depends on the activitv of end organs, the stimulation of which produces centripetal impulses that lower the central excitatory state. That the lengthening reaction does not involve the abolition of central excita-



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Myotatic Reflexes in Synpathectomised Muscle. 425

tion with the consequent production of a state of temporary central inhibition may be seen in fig. 15, Plate 23. A " silent period " in the galvanometer striing record is neither an index nor a characteristic accompaniment of the lengthell- ing reaction. Both in normal and in sympathectomised muscle string activity is a constant concomitant of the lengthening reaction. It is early in the application of tension that a difference is to be noted in the electric responses from niormal and sympathectomised muscle. In the normal muscle complete asynchronous activity of' the string record is seen throoughout the application of tension both at low and at high threshold. This is a characteristic feature of myotatic contractioni in normal muiscle subjected to evenly increased stretch unless the rate of stretch is sufficiently great to elicit a musele jerk. In sympathectomised muscle this asynchronous activity is seen only at high threshold of applied tension, fig. 15, Plate 23. At low threshold, on the other hand, there is to be seen the combination of large compound waryes aind short " silent periods " which have already beeni taken as eviden ce of incompletely synchronised firing in two or more muscle fibre units. This is no doubt due to the simultaneous activity of low threshold receptors in their firing into the miotoneurone pool. The asynchronous activity of norma,l muscle suggests the presence in it of a group of stretch-excitor end organs which are evenly distributed over a stiiulation threshold gradient. The low threshold receptors are so excitable that they respond to minimal amounts of stretch although they produce firing at the slow rate of 9 to 11 per second. It has been observed that in sympathectomised muscle these low threshold recejptors still produce firing at the same rate, fig. 6, Plate 22, but that at a slightly higher threshold a group of receptors are brought into activity together.

On such evidence it is submitted that sympathectomy has produced a dis- tarbance of the even distribution of stretch-excitor end organs over a threshold gradient in such a way as to produce, by increasing the excitability of a inumber of receptors to the same or almost the saime level, a concentration at low threshold of end organs having the same or almost the same excitability. Such an hypothesis, which it is attempted to represent diagrammatically in fig. 2, serves to explain all the changes in proprioceptive reflex activity which have been described to follow the removal of the sympathe-tic innervation.

Concluding Remarks.

The changes in postural reflex activity following the removal of the sympathetic innervation to skeletal muscle in both niormal and pathological states may now be considered briefly.

vOL. cX,--B. 2 X



426 G. Phillips.

In the niormal animal no change in posture and proprioceptive reflex activitv is seen. The loss of maintenance of postural contraction which has been shown to be present in chronic sympathectomised inuscle is in the normal animal most probably compensated by the striking of a new balance in the fractions of the

I~~~~~~~~~~

RECEPTORS EXCITED

FIG. 2.-A x B normal threshold gradient of receptors exciting myotatic contraction in soleus muscle. A x Y -threshold gradient following sympathectomy. A stretch " OS " which in normal muscle activates " OM " exciting receptors, activates " ON " suLch receptors all at low threshold in sympathectomised muscle.

body weight supported by the myotatic contraction in the extensor muscles of the limbs of opposite sides. The difference in the amplitude of the knee jerks is masked by the isotonic nature of the contraction and particularly in large animals by the inertia of the limb. In the normal animal with intiact extero- and proprioceptors, -which, during examination of the animal, contribute an irregular stream of conflicting centripetal impulses to the motoneurone pool, a rapidly alternating state of just supraliminal and jitst subliminal excitation, shown to be characteristic of clonus in sympathectomised muscle, is prevenLted.

It will be remembered that the clinical changes following sympathectomy, described by the author, have been observed after intereollicular decerebration. By thus removing supracollicular inhibition and by the symmetrical disposition of the animal during its examination an attempt has been made to produce in the motoneurone pools of the extensor muscles a relativelv constant subliminal excitatory state. Such a condition has permitted the detection of slight constant differences in the qtuantitative value of centripetal streams of proprioceptive impulses.

It is believed that in man also, in pathological states producing a complete or partial removal of supracollicular inhibition and associated with an intact




vestibulo-spinal mechanism, slight constant changes in postu-tral activity may

be detected following sympathectomly. On. the basis of the hypothesis suggested above, one may expect an earlier disappearance of extensor spasm in

the sympathectomised limb) when it is forcibly flexed, due to the earlier onset of the lengthening reaction. No change in the amplitude of the spastic knee

jerk would be anticipated, but following sympathectomy one would expect the

spastic limb to fall into partial flexion following the phasic response of the knee jerk and not to remain in the partially extended attitude characteristic of it

before the operation. Such a fall is due to the production of the lengthening reaction in the spastic sympathectomised extensor by the kinetic stretch applied to it by the weight of the heavy leg falling immediately after the

upward fling of the knee jerk. For the reasons given before clonic movements would not be expected to be any more conspicuous after sympathectomy than before it.

In conclusion it is suggested that the term " tonus," whose meaning has become so gross, should not be used and that the results of the clinical examination of resistance in spastic extensor muscles should be stated in terms of that proprioceptive reflex, the lengthening reaction.

Sutmmary.

Changes in the proprioceptive reflex activity of skeletal muscle follow the removal of its sympathetic innervation. These changes are progressive and are most prominent some weeks after operation.

The myotatic tension produced in sympathectomised muiscle by kinetic stretch may be modified by varying the rate of application of stretch, there

being a critical rate at which the same amount of stretch elicits the same myotatic tension in both normal and sympathectomised muscle; at rates greater than this the sympathectomised muscle attains the greater tension and vice versa.

UTnder static stretch chronic sympathectomised muscle is unable to maintain

a postural contraction of other than low tension. Chronic sympathectomised muscle displays a marked tendency to exhibit

rapid clonic movements of low tension at all grades of postural tension of which it is capable.

The muscle jerk following sympathectomy displays a greater mechanical tension, a larger action current wave and a longer " silent period."

It is suLbmitted that these changes may be explained by a concentration at low threshold of the activity of those proprioceptive end organs which excite

2 H 2



428 G. Phillips.

myotatic contraction. Such an hypothesis differs considerably from the view expressed in a previous publication (Phillips, 1931) in that it is now believed that proprioceptive inhibition is coniditioned by the nature of the centrifugal firing rather than by the amount of applied stretch.

Finally it is concluded that in postural contraction sympathetic axones have no direct ef[erent influence on skeletal muisele fibres and that, the progressively cumulative changes which succeed syinpathectomy depend on some trophic alteration modifying the responses of proprioceptive end organs.

Acknowledgenents.

I am deeply indebted to Sir Charles Sherrington for his invaluable advice, for the laboratory facilities placed at my disposal and for his criticism of this paper. Mly thanks are due to Dr. R. M. Carletoni for the expert assistance rendered by him at aseptic operations.

REFERENCES.

Denny-Brown, D. (1928). " Reflex Posture," Bodleian Library, Oxford.

Denny-Brown, D. (1928). 'Proc. Roy. Soc.,' B, vol. 103, p. 321; vol. 104, p. 252.

Eccles, J. C., and Sherriington, Sir Charles (1929). 'J. Physiol.,' vol. 69, p. 1; 'Proc. Physiol. Soc.,' Decenmber 14.

Fulton, J. F., and Liddell, E. G. T. (1925). 'Proc. Roy. Soc.,' B, vol. 98, p. 577. Hunter, J. I., and Royle, N. D. (1924). "Surgery, Gynwcology, anld Obstetrics," p. 721.

Liddell, E. G. T., and Sherrington, Sir Charles (1924). 'Proc. Roy. Soc.,' B, vol. 96, p. 212.

Phillips, G. (1931). 'Brain,' vol. 54, p. 320; 'Med. J. Australia,' May 23. Philippson (1905). ' Trav. Lab. Inst. Physiol. Brux.,' vol. 7. Royle, N. D. (1924). 'Med. J. Australia,' January 26. Sherrington, C. S. (1909). 'Quart. J. Exp. Physiol.,' vol. 2, p. 109.

Sherrington, Sir Charles (1928). 'J. Physiol.,' vol. 66, p. 175; 'Proc. Physiol. Soc., July 14.

DESCRIPTION OF PLATES.

All figures read from left to right except figs. 10 and 16, which read in the reverse direction. Unless otherwise stated, time is indicated by a tuning forl vibrating at 100 d.v. per second. The myograph records appear as bright lines, the central line when present indicating the base line of zero tension. Tension in the torsion wires is indicated by deflection of the miirror beams away from the base line.

The table fall is indicated by a descending black line at the top of the figure. All measurements were made from the original plates.



Myotatic Reflexes in Symtpatthectomised lMuscle. 429

PLATE 21.

FIG. 1.-Bilateral soleus preparation-; sympathetic ininervation intact on both sides; single muscle fibre unit firing in each soleus before onset of stretch; both firing at rate of 10 per second; table fall - 3 mm. in 0 25 second. Nolte tension ascent is smooth and at same rate on both sides with attainment of approximately the same final plateau tensions. The electric responses commence 5 sigmia late on left side (below); they are conmpletely asynchronous on both sides and of the same order of magnitude.

FIG. 2.-Bilateral soleus preparation. Botb sympathetics excised; both strings " silent before table fall of 3 mm. in 0*23 second. Note unsteady rise at same rate on both sides to samie maximum tension with subsequent fall of both plateau tenisions.

(Sympathectomy 62 days previou sly) ; tension scale as in fig. 1. The electric responses commence 4 sigma late on the left side (below). Note short " silent periods " in both strings.

FIG. 3.-Bilateral soleus preparation; normal soleus records on the sa:me side as the time marker which is a 10 d.v. per second fork. Left soleus sympathectomised 52 days previously; table fall --4 mm. in 0 2 second; tension scale as in fig. 10.

FIG. 3A.-Bilateral preparation; faulty fixation of base line mrirror which is deflected 2 mnm. toward normal side; normal soleus records oni same side as the fa,ll indicator ; acute left sympathectomy 3 hours previously; table fall - 3 mm. in 0 2 second. Electric responses commence 48 sigma late on normal side. Note greater laximuLim tension on sympathectomised side only noderately well maintained. Note short " silenat periods " in sympathectomised muscle durinig application of stretch.

FIG. 4.-Bilateral preparation; normal soleus records on same side as the fall indicator; acute left sympathectomiiy 2 hours previously; table fall = 2 nmm. in 0 12 second. Electric responses appear 56 sigma late on normal side.

PLAT:E 22.

FIG. 5.--Bilateral preparation; right soleus, synmpathectomised 25 days previously, records on the same side as the f all indicator; table fall -- 3 mm. in 0 - 26 second.

FIG. 6.-Bilateral preparation; left soleus (lower string record) sympathectomised 15 days previously; single muscle fibre unit fires in. each muscle at rate of l 1 per seconid under the stretch provided by 2 gm. weight suspended fromn each tendon.

FIG. 7.-Same preparation as in fig. 6; record of firing set up by replabeing 2 gin-. weights with 10 gm. on each tendon.

FIG. 8.-Bilateral preparation ; soleus jerks elicited by electromagnetically released myograph; right soleus (recording above) synipathectomised 23 days previously ; " silent periods "--on normal side 0 - 12 second, on operated side 0 * 18 second. Note inconmplete clonus following jerk in the sympathectomised muscle.

FIG. 9.-Bilateral preparation ; soleus jerk.s produced by lightly tapping the fall table with a rubber-covered brass rod. Sympathectomised soleus records onr same side as the tuning fork; two jerks shown were elicited by tappinig the table at widely separated points; tension scale as in fig. 8.

FIG. 10.-Single soleus preparation; highiest record produced by a table fall of 4 mnm1. in 0 2 second. Lowest record indicates passive tension developed by the same fall at the same rate after section of the motor nerve (8 per cent. of the tcotal); intermediate record shows passive tension developed by same paralysed soleus if the stretch be increased to 7 mm. at the sanme rate (36 per cent,. of the total).



430 Myotatic Reflexes in Sympathectomised Muscle.

FIG. 11 .-Bilateral preparation; soleus jerks elicited by electromagnetically released nyograph; right soleus, recording above, sympathectomised 23 days previously; " silent periods "-on nlormal side O*07 second, on opera,ted side O 12 second. Tension scale as in fig. 8.

PLATE 23.

FI-G. 1.2.-Bilateral preparation; right soleus, recording above, sympathectonmised 25 days previously; table fall equals 3 mmn. in 1 3 seconds. Note the greater tension developed by the normal soleus.

FIG. 13.-Same preparation as in fig. 12; same amount of stretch at a faster rate, 3 mm. in 0-19 second. Note the greater tension developed by the sympathectomised soleus.

FIG. 14.-Bilateral records of clonus; sympathectomised muscle records above; rate on normal side 15 per second. Fast rate on sympathectomised side approximately 50 to 60 per second. Time as in fig. 11.

FIG. 15A.--Clillical lengthening reaction produced in sympathectomised muscle by a gradually increasing tension applied to the tendon (soleus operated 28 days previously); fall of signal indicates onset of lengthening reaction.

IAG. 15B.-Lengthening reaction elicited in a normal soleus by the same method. These two records were made successively and are not comparable in point of time.

FIG. 16.-Philippson-type reflex (soleus exciting-soleus reacting). Contraction of sympathectomised soleus recorded below; tension scale as in fig. 12.

FIG. 17.-Control mvogram of soleus jerk elicited in normal bilateral preparation by electromagnetically released myograph. Taken at a relatively high initial tension and displaying the maximum observed disparity of 0 019 second in the " silent periods" of two normal soleus miuscles.



myotatic reflexes in sympathectomised muscle

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