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258

Observations on Concurrent Contraction of Flexor Muscles in the Flexion Reflex.

By R. S. C

, Fellow of New College, and Sir C

S

,

0 . M., F.R.S.

(Received June 16, 1926.)

[Plate 8.]

The “ flexion reflex,” flexing the limb (hind) at hip, knee and ankle, is elicit- able from any one of a number of the various afferent nerves of the limb. It reveals to inspection little difference whichever be the particular afferent nerve stimulated. That the flexion evoked cannot, however, be strictly the same under excitation of the several different nerves has been already shown (5). To examine further the differences it thus presents as evoked from the several nerves we have taken simultaneous myograms from paired flexor muscles under provocation of the reflex from various different afferent limb-nerves.

The muscle pairs selected have been (1) a hip-flexor and a knee-flexor (tensor fasciae femoris and semitendinosus) together, (2) a hip-flexor and an ankle- flexor (tensor fasciae femoris and tibialis anticus) together, and (3) a knee- flexor and an ankle-flexor (semitendinosus and tibialis anticus) together.

1. —Method.

The preparation (cat) has, after spinal transection in the anterior lumbar region and immediately subsequent decerebration under deep anaesthesia, been made ready for the myograph by appropriate isolation of the test muscles.

The method of fixation and attachment to the myograph has been as described in previous communications, except that for tibialis anticus the freed tendon has been passed round a small light pulley allowing in its case a horizontal pull on the myograph. The resting tension of the two muscles has been adjusted for near equality. In using tensor f. femoris for the myograph distinction was made between its long anterior portion, tens, f. fern, longus, and its short posterior portion, tens. f. fern, brevis. Most of the observations with it were made on the former, the tens. f. f. brevis being cut away, though not always to equal extent. The myograph employed is of isometric pattern and records optically : its description is given as an Appendix to this paper ; it is a further modification of the myograph described in a previous communication (6). The afferent nerve,

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bared and cut, has been stimulated by single or double-shock series of various frequency delivered from a coreless coil fed by a 2-volt battery.

II.—Results.

There is, commonly, marked difference of strength between the contractions concurrently given by the pair of muscles, Plate 8, fig. 1. This might mean that of the two muscles one was a more powerful unit than the other, and th at the afferent nerve reflexly activating them did so simply in the same proportion for both. The differences observed cannot, however, be fully accounted for in that way. The ratios between concurrent contractions of the same muscle- pair differ widely as yielded by different afferent nerves in one and the same preparation. Thus, in the same experiment and in almost immediately conse­

cutive observations, hip-flexor and ankle-flexor being the muscle-pair employed and the following afferents stimulated successively at the same coil distance, internal saphenous nerve evoked from tensor femoris 660 gm. contraction concurrently with 950 gm. from tibialis ; popliteal nerve evoked from tensf.f. 190 gm. contraction concurrently with 1120 gm. from tib. ant. ; external cutaneous nerve evoked from tens. f . f . 1510 gm. concurrently with 450 gm.

from tib.ant. ; and a digital branch of musculo-cutaneous nerve evoked from te n s .f.f. 195 gm. contraction concurrently with 1370 gm. from ant. The connection with a given flexor muscle is evidently different quantitatively for different individual afferent nerves of the limb (cf. text figure and fig. 1, PI. 8).

Assessing the concurrent contractions by the tension-values developed in each, and stating that of the weaker as percentage of that of the stronger, instances of the ratios found, under stimulation not far from maximal for the afferent nerve, have been as follows :—

Observations on Concurrent Contraction o f Flexor Muscles. 259

Afferent Nerve. Hip-flexor.

Tens. f. f.

j

Knee-flexor.

Semitend.

Ankle-flexor.

Tib. antic.

External cutaneous .... ....

l

100 100

23 (much 17

variation) 30 30 Internal saphenous .... ... -j

l

100 100

56 55

87 87 Nerve to sartorius ... 100 37

Superficial obturator .... ^ 100 62

62 3

Nerve to quadriceps extensor .... ^ 100

13 21

21

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260 R. S. Creed and Sir C. Sherrington.

Afferent Nerve. Hip-flexor. Knee-flexor. Ankle flexor.

Tens. f. f. Semitend. Tib. antic.

r ^{42 100}

Popliteal nerve .... 1 12 100

i 3 (or less) 42

Peroneal nerve ....

66 100

Peroneal nerve distal to tib. ant. { ^{14 100 69 69}

Digital branch of musculo-cutaneous ^ 9

93

100 100

I t was noticed th at fluctuations of reflex activity in one and the same experi­

ment did not greatly disturb the ratio obtained between strengths of the reflex responses of the two test muscles. The ratios were, however, found to vary considerably from experiment to experiment. Thus, in one experiment, int. saph. nerve evoked 12 per cent, stronger contraction from semitend. than from tens. fasc. femoris. In regard to tensor fasciae femoris this is traceable in part to the resection of the posterior short portion of the muscle in order to avoid th at portion’s lying slack under the initial tension applied in the resting position. The proportion of the muscle resection could not always have been the same. Variation of some of the ratios from experiment to experiment may in part be due to the well-known frequent segmental variation of the lumbo­

sacral plexus from individual to individual. In one preparation hamstring nerve evoked no response from ten. f. f. longus ( . 5), in three others it did evoke a weak response. Occasionally in one and the same experiment the ratio given under the same coil stimulus applied at different times to the same nerve varied considerably: thus digital branch of musculo-cutaneous yielded at one time semitendinosus contraction as 93 per cent, of tibialis anticus and at another 111 per cent.

One factor influencing the ratio was found to be the strength of the stimulus applied to the afferent nerve. With increase of the strength of the stimulus the strength of the reflex contraction commonly increases in both muscles but the increments do not maintain the same ratio. T h u s: with internal saphenous n erv e:—

Stim. in cm. on coil 22 20 18 16 14 13 12

Tib. antic, grm. tens. .. 90 225 290 310 750 860 860 Tens. fasc. fern. gm. tens. . 380 610 700 620 900 980 1090

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Observations on Concurrent Contraction o f Flexor Muscles. 261

Coil in cm. . . 18 15 14

Semitend. gm. tens. . . 25 150 210

Tens. f. fem. gm. tens. 600 830 970 »

Coil in cm. ^{. .} 28 24 20 16

Semitend. gm. tens. . • 0 90 224 488

Tens. f. fem. gm. tens. 50 1265 1380 1760

Coil in cm. .. 25 24 22 20 18 16 14 13 12

Semitend. gm. tens 20 50 90 170 215 300 510 460 500

Tibial. ant. gm. tens. 30 110 240 390 480 630 750 730 750 Again, with nerve of quadriceps extensor muscle

Coil distance in cm. .

20 18 16 14 13 12

Tib. antic, gm. tens. .. . . 30 60 75 170 230 360

Ten. f. fem. gms. tens. 250 660 820 1140 1330 1470

Again, with external cutaneous nerve of thigh :—

Coil dist. in cm. .. .. 25 24 23 21 20 19 18 16 14 13 12 Semit. gm. tens. .. 0 0 4 13 9 20 16 14 125 233 250 Tens. f. fem. gm. tens. .. 0 some 80 160 330 390 510 530 1530 1870 1980 In such instances the ratio of the less contracting muscle to the more con­

tracting muscle somewhat steadily increases with increase of the stimulus strength. Where, however, the afferent is of more equal power upon the two paired muscles cases such as the following are m e t d i g i t a l branch of musculo-cutaneous of peroneal:—

Coil in cm. 24 23 22 20 18 16 14 13

Tib. ant. gm. tens. 30 25 65 360 590 710 790 1040

Semitend. gm. tens. 35 60 90 330 560 630 860 1160

Here ankle-flexor along a certain range of stimulus gave the stronger contraction, although either side of that range it gave the weaker.

Again, with peroneal nerve :—

Coil in cm. 20 19 17 15 14 13 12

Tens. f. fem. gm. tens. 30 90 420 550 500 510 600

Semitend. gm. tens. 30 130 400 770 690 840 820

Coil in cm. . 16*5 16 15 14-5 13*5

Tens. f. fem. brevis gm. tens...

. 35 200 320 390 490 Semitendinosus gm. tens.

. 60 200 400 580 1010

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262 R. S. Creed and Sir C. Sherrington.

Similarly, in other instances, with peroneal nerve the increments in semiten- dinosus were relatively greater than in tens. f. f. with strong stimuli, and conversely with weaker.

That each increase of stimulus calls forth commonly an increment of con­

traction in both of the paired muscles indicates that among the motor units of each of those muscles are some which for the particular afferent nerve stimulated respond at like reflex threshold. We have in several instances sought to determine how far this equality of reflex threshold extends toward the limit of minimal stimulations of the afferent nerve. Naked eye inspection of bared muscles had already shown (5) that in this, the flexion-reflex, separate flexor muscles present differences of minimal threshold which are but slight under excitation from one and the same afferent nerve. The double myo­

graph gave opportunity for better examination of this point in regard to the test muscles here taken, although the well-known variability of minimal reflexes presents difficulty.

Instances of comparison :—

Aff. nerve.

Peroneal

Muscle pair.

Tens. f. fern, and semitend.

Coil distance in cm.

22 cm. neither 21 cm. both.

33

33

3 3

17 „

16*5 „ „

33

18-5

18 „ „

Ext. cutan. .. ,, ,, „

n. of sartorius.. ,, ,, ,, Int. saphenous ,, and tib. anticus

3 3 3 3 3 3 33 33

n. of quadr. ext. ,, ,, ,, Int. saphenous tibialis ant. and semitend.

Digit, of muse, cutan. ,, ,, ,,

25 cm. neither ; 24, t. f. f. only, 23, both.

26 cm. neither 25 cm. both.

25 „ „ 22 „ 20 „ 26 „ 25 „

3 3

3 3

33

With internal saphenous in separate experiments the minimal reflex threshold for tibialis anticus was sensibly similar to that of tensor f. fern, on the one hand and of semitendinosus on the other, indicating that for this afferent the reflex minimal threshold was sensibly the same for hip-flexor, knee-flexor and ankle- flexor. For one and the same afferent nerve the inferior limit of its reflex threshold *for concurrent contractions of each of the two test muscles has in the case of a number of the afferent nerves proved closely alike, perhaps identical.

Yet for certain other afferent nerves that seemed not to be the case ; thus, it was doubtful whether in the case of popliteal nerve its threshold of reflex

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action on tensor f. femoris is usually nearly so low as for semitendinosus ; and other instances have met us.

Observations on Concurrent Contraction o f Flexor Muscles. 263

Text-figure.

—Concurrent reflex contraction of hip-flexor T . f . f . and knee-flexor $£. in response to stimulation of ipsilateral peroneal nerve by single-shocks a t 45 p.s. a t 13 cm. coil distance. Tendon movement X 205 for each m uscle: tension-develop­

ment 200 grm. p. cm. ordinate ; initial tension about 60 gm. for each muscle. S, shadow of short-circuiting key for stim ulating circuit. Time in 1/50 sec.

The mechanical latency of concurrent contractions given by the paired muscles has not shown large difference as between the members of the pair. In some observations on hip-flexor and knee-flexor as test muscles the speed of the record­

ing plate has allowed comparison of the latencies to an error of ± 1 • 5 There, with internal saphenous as afferent, the greatest difference of latency between tensor f. fern, and semitendinosus was 3 a, the hip-flexor being in every instance

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264 H. S. Creed and Sir C. Sherrington.

the earlier. With external cutaneous nerve the greatest difference was 6 <

, tensor f. fem. was always the earlier (Plate 8, figs. 1 and 2) ; with peroneal nerve the maximal difference was 4 a and tensor f. fem. always the later (text- figure) ; with obturator nerve the greatest difference was 6 a and tensor f. fem.

always the earlier.

With hip-flexor and ankle-flexor as pair, the travelling surface used allowed readings not closer than ± 2 • 5 a ; the response of tibialis anticus, the tendon of which acted round a light pulley, was with all the afferents found to be the later, but very rarely by more than 5 a. When paired with semitendinosus it was also, with all the afferents tried, the later ; but in three instances by less than 2 a, subject to the latitude ± 2*5 a of the reading.

That the above-instanced similarity both of reflex threshold and of latent period obtains for the concurrent contractions of the test muscle pairs amounts to the afferent nerve commonly bringing into play, with like facility and like time-relations, motor units widely scattered in the limb, irrespective of the circumstance th at many of them lie grouped in separate and even distant individual muscles. From the point of view of the afferent nerve the muscular entity executing the reflex movement is in so far not this or that muscle but a composite aggregate of motor units, scattered through and forming parts of a number of separate and even distant muscles. This composite collection is given functional solidarity and homogeneity by the likeness of threshold and latency obtaining among its units in regard to the afferent nerve which brings them into action. An increment of stimulus does not break this homogeneity but merely brings to it a certain addition again composed of units mutually similar in threshold and latency although made up from muscles anatomically separate. The individual muscle, although an anatomical entity, does not of itself and as one whole offer such reflex unity as does the above anatomically heterogeneous group ; nor does the individual muscle as such constitute a functional unit of the kind into which analysis of co-ordination resolves the motor apparatus executive of the reflex movement.

In the performance of a spinal reflex act therefore the executant muscular entity is not this or th at individual muscle but a set of motor units made up from parts of various muscles. In carrying out this principle the several afferent nerves, although all severally evoking limb-flexion, combine the com­

ponent part-contractions of the confederate muscles in proportions and degrees which are different and more or less characteristic for each individual afferent.

The flexion-reflex is thus not wholly the same when evoked by different afferent nerves, even under comparable strengths of stimulus. The contraction of these

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Observations on Concurrent Contraction o f Flexor Muscles. 265 or those particular flexor muscles is stressed according as the elicitation of the reflex is by this or that particular afferent nerve (5).

The term “ flexion-reflex ” therefore, just as the term “ scratch-reflex,”

denotes, strictly speaking, a group of reflexes all more or less alike and all using approximately the same motor apparatus in approximately the same way, yet from one afferent to another differing in detailed distribution of the motor units employed, while yet always conforming to the general type “ flexion-reflex ” (7).

I I I .—Other Features.

Some features of these contractions concurrently provoked in the paired flexors seem of interest, aside from the main theme here dealt with. (1) The reflex after-discharge has been, with much regularity, despite variety of afferent nerve employed, more prolonged from semitendinosus and tibialis anticus than from tensor fasciae femoris. In semitendinosus although prolonged it usually presents a sharp decline at outset. Where the after-discharge has taken the form of a stepped decline, we have observed very strict synchronism in the steps of the simultaneous records from the two muscles. (2) The rate of the stimulation has sometimes been low, i.e., 45 single shocks a second ; the reflex contraction of both muscles has then usually shown the stimulus rhythm with marked and about equal distinctness (see text-figure), but in some experiments one muscle and not the other has shown the stimulus rhythm. (3) Instances have occurred where the wreaker contraction of a paired response has already begun to decline before the period of rise of the stronger fellow contraction has reached halfway. The weaker contraction has sometimes subsided altogether, despite continuance of the stimulation of the afferent nerve, at a time when the stronger contraction shows little or no decrease.

IV.—Summary.

The relative amount of contraction concurrently excited in pairs of muscles flexing hip, knee and ankle, under stimulation of this or that different afferent nerve, is examined and shown to be different and more or less characteristic for each several nerve.

Each afferent nerve possesses motor units, which in regard to itself are of practically similar threshold, scattered apart in separate and even widely distant muscles of the limb ; and the latency of mechanical response of these is closely similar. The executant entity in the reflex is thus not this or that muscle but a composite collection of motor units, made up from portions of anatomically separate muscles.

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266 R. S. Creed and Sir C. Sherrington.

With concurrent reflex contractions of two flexor muscles the after-discharge may, as between the two, differ considerably in amount although the stimulus for both is one and the same.

V.—Appendix.

By Sir C

S

, F.R.S.

The isometric myograph employed was a modification of that described in a previous communication (6). I t has advantages of greater magnification of the muscle-shortening, and therefore closer approximation to pure isometric record and employment of smaller angular torque of the steel resistance. Moreover, the instrument provides simultaneous records from two muscles, against either equal or different resistances and under adjustable initial tensions.

The arrangement is as follows : The magnified image of an illuminated narrow rectilinear slit, similar in pattern to a spectrometer slit, is thrown through the horizontal slit-opening of an ordinary cardioelectrograph camera (Cambridge Scientific Instrument Co.) upon a falling photographic plate. The magnified image is obtained by a low-power microscope objective, in front of which, after the beam has been deflected by a prism, two little mirrors, one attached to each of the twin wires forming the double myograph, receive the image and reflect it separately to a second prism which deflects the thus paired images through a cylindrical lens condensing them upon the camera plate. Torsion of either wire displaces its member of the image pair horizontally on the vertically moving photographic plate. For torsing the wire the muscle is attached to a lever arm 10 mm. long fixed at right angles to the wire’s axis at a given distance from the clamp holding the wire. The lever arm has points for attachment of the muscle at one-third, two-thirds, and full length of the arm. The excursion of the focussed image on the photographic plate amplified the excursion of the lever arm at these three points 560, 310 and 205 times respectively. Excursion of the image completely across the recording plate involved in all the three cases a torque of the wire of less than 3°. Within the range of torsions employed the excursion of the images for equal increments of pull (tension) was sensibly equal. The actual values of the tension scale were suitably adjusted by employ­

ing steel wire of different diameter without alteration of length. The range of tension scale employed varied from 1,000 grms. per 18 mm. excursion of the image to 100 grms. per 24 mm. excursion.

The natural vibration period of the myograph was in no case less than 1600 per sec. The damping was high ; under sudden release (by breaking of the

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Creed and Sherrington. Roy. Soc. Proc., B, 100

PI. 8

[Facingp. 267.

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muscle-tendon) from a tension of 5 • 5 kilos, and an excursion of 910 mm. magnify­

ing 560, the image was steady again at zero in rather less than 0-015 sec.

With this arrangement a tetanic contraction developing as mu&h as 6 • 5 kilos, and yielding a record of more than 110 mm. excursion on the plate permitted movement of the muscle-tendon by only 0 • 2 mm., less than 0 • 2 per cent, of the length of the hip flexor employed or knee flexor employed, and less than 0-1 per cent, of the length of ankle flexor employed.

I am indebted to Mr. J. O’Neill of this Laboratory for his care and ingenuity in execution of the myograph. Its mirror device is similar in principle to that of Keith Lucas (3, cf. also 1, 2) for registration of isotonic contractions in excised frog muscle.

For recording time a Rayleigh magnetic wheel was used, revolving between the light source and illuminated slit, thus breaking the myographic image 50 times a second. Signal records were given by attaching to the armature of an electromagnet key which shorted the stimulating circuit, a mirror illuminated from a separate light source but focussing its image upon the recording plate.

R EFEREN CES.

(1) Blix, ‘ Skandinav. Arch. f. Physiol.,’ vol. 5, p. 185 (1895).

(2) Brodie and Richardson, ‘ Jnl. of Physiol.,’ vol. 30, p. 443 (1897).

(3) K eith Lucas, ‘ Jnl. of Physiol.,’ vol. 21, p. 353 (1904).

(4) Langley, ‘ Jnl. of Physiol.,’ vol. 12, p. 347 (1891).

(5) Sherrington, ‘ Jnl. of Physiol.,’ vol. 40, p. 28 (1910).

(6) Sherrington, These ‘ Proceedings,’ B, vol. 92, p. 245 (1921).

(7) Sherrington, ‘ Integrate Action of the Nerv. System,’ London and New York, p. 127 (1906).

DESCRIPTION OF PLATE 8.

Concurrent contractions (isometric)- of hip-flexor, tensor fasc. (T. f .f .) and knee- flexor, semitendinosus (St.), in spinal flexion reflex (cat), evoked from nerv. externus.

Fig.

1.—Tensor f. fern, develops 2210 gm. tension, semitend. develops 710 g m .; tendon movement magnified by 310 for tens. f. f. ; 560 for semitend. Stimulus, double shocks 90 a sec. a t 14 cm. coil distance ; stimulus period signalled (

.) direct by shorting key on plate. Time marked in 0-02 sec. by breaks in myogram line. Initial tension for both muscles approximately 40 gm. Time-relations of development of the plateau and of after-discharge are seen to differ between the two muscles.

F

. 2.—Similar to above, but stimulus a t 15 cm. coil. Tendon movement magnified by 205 for tens. f. Jem. with tension of 200 grm. per cm. ordinate, and by 310 for semitend.

with tension of 62 gm. per cm. ordinate. Initial tension about 30 gm. for tens. f. / . , about 20 gm. for semitend. The reflex latency of the mechanical response is for both muscles nearly the same, but th a t of semitend. is the longer.

Observations on Concurrent Contraction o f Flexor Muscles. 267

VOL. C.— B. X

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