The Interaction between Two Trains o f Impulses Converging on. (Communicated by Sir Charles Sherrington, F.R.S. Received June 25, 1929.
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1 The Interaction between Two Trains o f Impulses Converging on the Same Moto By Sybil Cooper, Research Fellow of St. Hilda s College, Oxford, and D. D e n n y -B row n, Beit Memorial Research Fellow. (Communicated by Sir Charles Sherrington, F.R.S. Received June 25, 1929.) (From the Physiological Laboratory, Oxford.) [Plate 13.] It was shown in an earlier paper (7) that if maximal stimulation of either of two different afferent nerves can reflexly excite fractions of a given flexor muscle, there are generally, within the aggregate of neurones which innervate that muscle, motoneurones which can be caused to discharge by either afferent (i.e., motoneurones common to both fractions). The relationship which two such afferents bear to a common motoneurone was shown, by the isometric method of recording contraction, to be such that the activation of one afferent, at a speed sufficient to cause a maximal motor tetanus when transmitted to the muscle fibres, caused exclusion of any added mechanical effect when the other afferent was excited concurrently. This default in mechanical effect was called occlusion. Occlusion may conceivably be due to total exclusion of the effect of one afferent pathway on the common motoneurone by the activity of the other ; but facilitation of the effect of one path by the activation of the other when the stimuli were minimal suggests that, in some circumstances at least, the effect of each could augment and summate with that of the other at the place of convergence of two afferent pathways. Further investigation, using the action currents of the muscle as indication of the nerve impulses discharged by the motoneurone units, has now given some information regarding the effect of impulses arriving at the locus of convergence by one afferent path when the unit common to both is already discharging in response to impulses arriving by the other afferent path. Our method has been to excite both afferent nerves in overlapping sequence by series of break shocks at a rapid rate and to examine the action currents of the resulting reflex for evidence of vol. cv. b. 2 E
2 364 S. Cooper and D. Denny-Brown. the appearance of the rhythm of the second series in the discharge caused by the first when the two series are both reaching the motoneurone. The myographic method, when used alone, revealed by the appearance of greater tetanic contraction tension whether further groups of motor units were excited by an additional afferent stimulus. The present experiments attempt to show, in motor units already in contraction, the alteration in motor discharge caused by an additional stimulus series to an additional afferent source in circumstances where no further mechanical effect occurs. In a selected flexor muscle the relation between the fraction in the motoneurone aggregate caused to discharge by a stimulus to one afferent, to that caused to discharge by another afferent is dependent upon the particular pair of afferents selected. For our present purpose it was essential to use a reflex discharge in which as many motor units as possible are common to two different afferents. It is obvious that if the second stimulus can excite some units which are not already excited by the first stimulus, i.e., if the second afferent path is not completely occluded, the action currents of these units will confuse the result by making it impossible to find which of the action currents caused by the second series have come from units already excited by the first stimulus, and which are from units directly excited by the second stimulus alone. It is necessary therefore to use a combination of afferent stimuli in which the second stimulus series is completely occluded mechanically, i.e., can excite no further reflex contraction in the muscle because the first stimulus has already excited to the utmost all the units available to the second. The degree of occlusion must therefore be controlled by a mechanical record, and the rate of repetition of the first stimulus series must be such that each unit excited is thrown into a reflex tetanus so completely fused that the mechanical effect of further excitations in it is negligible. The rate must, however, be as slow as this necessity will permit, in order to leave sufficiently long periods between waves to allow the excitation waves from the second series to be recognised. In practice the leading stimulus fulfilled these conditions if formed of repetitive break shocks at a rate of about 50 a second. To find the condition of the motoneurone resulting after one excitation by the first series, as tested by a member of the second series, it is most useful to have each repetition of the second series occurring at a different time relative to the occurrence of the excitations of the first series. This was secured by arranging the second stimulus to be one of repeated excitations at a rate differing from the rate of the first by only a few excitations a second ; so that when
3 Impulses on Motoneurone. 365 the two trains of stimulus together played upon the same motor units each succeeding excitation of the second train altered in temporal relationship with the corresponding excitation of the first train, until the two coincided in time and then again separated. The rates of the two trains of stimulus were thus arranged to beat at periods varying from two to eight times a second. Method. The preparation used was identical with that described in the earlier paper, that is, it was a decerebrate cat made spinal by cord transection in the first lumbar region. Two muscles were prepared, semitendinosus and tibialis anticus, the former of these was found to give a very much better result (fewer confusing secondary waves) so that in the later experiments it only was used. Various afferent nerves in the same limb were prepared for stimulation and the rest of the limb immobilised by nerve and tendon section. Adequate drills and clamps were used for fixation. The muscle was attached by means of a ring and steel hook to a torsion wire myograph of high natural frequency and was recorded isometrically. The electrical responses were recorded by a string galvanometer of the Cambridge type whose fibre was in the same optical system as the myograph. The stimulation was by means of two torsion-wire keys, delivering slightly differing rates of equal break shocks at frequencies of about 50 a second. The leading-off electrodes were fine pins of the Ag : AgCl type ; the responses were largely diphasic, but sometimes K 2H P04 (Buchanan (5)) was injected near the distal electrode to make them monophasic. An indication of the limitation of the method by peripheral factors is shown in the effect of one such stimulus upon another, when both are applied to the one motor nerve so that no central synaptic junction is involved. These effects will be described first. Results. (a) Motor nerve stimulation. Applied to the motor nerve two trains of repeated break shocks of differing rate of repetition cause, if each alone can excite the muscle to its maximum, a motor tetanus, whose action currents reflect the interference between the two series during the period of double stimulation (fig. 1). With these conditions the alternations in action current rhythm are clearly the result of the effect of the refractory period in the nerve in diminishing or abolishing the second excitation when it falls within that period. The method is to estimate the difference in time between a member of the hrst train of break shocks and the corresponding member of the second series when the change in the muscle action currents shows that the second member 2 e 2
4 366 S. Cooper and D. Denny-Brown. of the pair is just able to stimulate. Since by the difference in the rates of repetition the members of the more rapid stimulus series are falling progressively earlier in relation to the members of the second series the responding muscle will, for a period before and after the moment when the member of one series occurs simultaneously with the member of the other series, reveal only single waves corresponding each to one wave of excitation ; as soon as the two stimuli separate by an amount greater than the refractory period the muscle action current becomes smaller and then obviously double. By the rhythmic variation in the relationship of each member of one stimulus series to the corresponding member of the other, the absolute refractory period can be calculated in the way which Beritoff (2), Brucke (3), and Briicke and Plattner (4) have used for the muscle-nerve preparation of the frog ; such calculations give results comparable with those yielded by methods of direct measurement of the action current of the nerve after two stimuli delivered at close intervals (Adrian (1), Forbes, Ray and Griffith (8), and Gasser and Erlanger (9)). In our results from mammalian muscle-nerve preparations the refractory period is measured from the first decline in the size of the large response after the centre of the phase of single waves (Plate 13, fig. 1) since this usually occurs before the second wave appears as a recognisable deflection ; it varies between a for fresh muscle with good circulation to as m for a preparation which has been on the myograph for some hours and has become cold. If the overlapping stimulus is repeated at a rate of about 50 a second the mechanical record sometimes shows the alternate simple and double responses by ripples upon the plateau. (b) Reflex stimulation. When the method is applied to reflexes it is in the first place essential to use an afferent for background which activates a large fraction of the total units of the muscle (6), to allow a greater possibility of complete occlusion of the second afferent. In the case of M. Semitendinosus the ipsilateral peroneal or saphenous nerves were most suitable, their large reflex response in the muscle occluding the reflex response of many other nerves. The second afferent was necessarily one which produced by itself a reflex of fair tension so as to have well defined action current; in each experiment it was found necessary to find by trial which afferents were totally occluded. It was arranged that the occluding stimulus series which caused the large overlapping response (this will be called stimulus A) began alone, and when the response reached its plateau the second occluded stimulus series (which adds nothing to the contraction except at intervals slight signs of double rate of discharge) was then released (this will be called stimulus B). Stimulus B
5 was allowed to continue alone for a short interval after the end of stimulus A so that in each record there was a short period of each stimulus alone separated by a period of overlapping stimulation by both A and B. Besides this, controls of the whole of each of A and B alone were taken shortly before and after the double stimulation. In the early experiments when rates of 49 and 41 a second for A and B respectively were used, it was immediately apparent that, during the period when the excitations of B fell in the intervals between the excitations of A, both trains of stimuli were exciting the motor units and causing a double rhythm (fig. 2). Here there are obvious signs of the second stimulus having produced excitation all through. Since at these rates the stimuli move in relationship to one another by 3 3 cr in each 1 /49th second, it must be the case that each member of the B series can excite the motor units already excited by A at least 3 3 cr earlier. One may conclude from this that, given a sufficiently long interval, stimuli from one afferent will not prevent stimuli from another from coming through, even though the mechanical record shows no increased tension. When the A stimulus was 51 5 a second and the B stimulus 47 5 a second (fig. 3) the shift in relation of any two excitations was about 1 64 cr in each 1/51-5 second. It is necessary to emphasize here that the conditions which concern us are those obtaining only when an excitation of B closely follows an excitation from A ; for A, being of greater mechanical effect than B, presumably excites some units not available to B all through. This means that attention must be directed to the decline of each beat of single waves when B is following A. From the period of double rhythm up to the middle of the phase of single rhythm the waves though they become single remain small. That is, we assume, the result of a small wave from A occurring in units not affected by B (which causes the main wave). Immediately the centre of the phase is reached a large wave usually occurs, owing to the coincidence of the two excitations. This large wave is not greater than that produced by A alone (in the control) and bears the same shape, therefore it can be assumed that here the effect is the same as of a single A excitation alone. In the second half of the phase of large waves each stimulus element of B is following each stimulus element of A, and it is seen that the resulting wave is immediately reduced in size. In these circumstances the reduction in size can only mean that the wave of B afferent excitation is producing a small afferent wave of excitation which is following the wave produced by A. The occurrence of this small B excitation of the motor units, judged by the diminu Downloaded from on October 22, 2018 Impulses on Motoneurone. 367
6 368 S. Cooper and D. Denny-Brown. tion in wave size, begins immediately following tbe large centre wave (as at xi in fig. 3). Now since the next wave after the large wave is produced by the arrival of the B excitation, not longer in fig. 3 than 1 64 a after the A excitation, it follows that the A excitation has not entirely prevented the B afferent wave from exciting the motor unit after the lapse of that period. When the centre of the period of large waves falls between two responses and therefore the next wave is caused by an A excitation followed by a B stimulus at a still shorter interval the wave is again smaller than an A maximal wave, and it is therefore possible that B has again caused an excitation. It occurs often that the following two or three waves are of the same size, and therefore it seems likely that the B effect is occurring the same interval after A each time. This is well seen at x2 in fig. 3, and here it is obvious that during this period the B excitations are falling at a maximum of 2 4 a, 4 1 and 5 7 a after the A excitations, and yet produce each a small disturbance arriving at an approximately constant interval (judged by the constant size of the combined wave) after the disturbance produced by the A excitation. Since in the first of these the afferent B wave of excitation must arrive at the motor unit 0 82 gafter the wave, it must fall within the absolu phase of the central portion of the motor unit, if that portion possesses a refractory period as long as that of its peripheral process (the motor nerve fibre). And yet the result is a wave of motor excitation which must arrive at the muscle after an interval at least as long as the absolute refractory period of the peripheral nerve. A similar case is seen at y in fig. 4, where the A and B responses probably coincide ; and as the rates are 49 and 47 a second the subsequent B stimuli fall 0 87 a, 1 74 the A stimuli. In order to make further enquiry into this probable delay of the effect of an early second stimulus to the motoneurone we used trains of stimuli at closer and more rapid rates, e.g., 66 and 64-5 a second. All preparations tried with these rates tended to a type of reflex discharge with large numbers of irregular secondary waves, which confused the interpretation through their effect in altering wave size. One feature sufficiently constant to be commented on was the multiple wave changes which we found with these rates. That is, instead of the rhythmic simple wave of variation seen in figs. 2 and 3 the motor discharge wave changed in form abruptly and regularly several times during a complete cycle of physical interference of the afferent stimuli (fig. 5). The most likely explanation of the phenomenon would appear to be the effect of afferent fibres of differing rate of conduction in the afferent
7 Impulses on M 369 nerves employed with resulting complicated wave interference. On account of this phenomenon we were not able to find further evidence of the delay of discharge effect of a stimulus arriving within 1 of another. Discussion. The results concern the effect of two afferent paths A and B converging upon a single efferent path. It is obvious from our results that afferent paths of equivalent sign do not join a neuxopile net with conduction in all directions, because the impulse from A would then traverse not only the network termination of B but would traverse B itself and render a stimulus to B ineffective, for a period at least equal to the time required for an impulse to traverse both A and B. Therefore the points of convergence must be regarded as being in some way discrete. The lack of refractory period at the point of convergence certainly indicates some simple type of convergence of the two afferents down stream in the reflex arc (i.e., probably on the final motoneurone). The flexor motor unit can be caused to discharge twice in as small an interval as the refractory period of the nerve fibre itself. Indeed there seems definite evidence that an impulse arriving by the afferent B, even though it comes during the refractory phase left by a previous excitation set up by A, can yet cause an excitation which arrives at the muscle after a period equal to the refractory period following the propagated excitation from A. This may conceivably happen in one of two ways, either the interneuronic locus has no refractory period at all following an excitation of the motoneurone by A and the excitation is deferred in the central portion of the motor unit mitil the peripheral portion has passed out of its absolute refractory phase, or else the whole motor unit becomes refractory after an excitation by A and the propagated disturbance arriving by B can be deferred at the point where B is contiguous to the motoneurone, until the latter has entered the period of recovery. This latter process would seem the more likely, since the phenomenon of central summation is exhibited by any one afferent alone and therefore B should possess some locus where excitation arriving by B is not immediately dissipated. The interpretation of a record such as is seen at x2 in fig. 3 is accordingly that the excitation from B is deferred for the first two or three waves until the refractory period of the motor unit, some 1-2 a, is passed and then causes an excitation. By the second or third wave the excitation from B is so late after A that it can be directly transferred from B to the motoneurone.
8 370 Impulses on Motoneurone. Summary of Conclusions. 1. When two afferent stimuli, each producing flexor excitation in a given muscle, are combined with the result that mechanically the second stimulus is completely occluded by the first, the electrical response shows that the second stimulus is affecting the motor unit even when no further mechanical contraction results. 2. When two afferent paths converge to cause excitation of the same motor unit each path is separated by an irreversibly conducting junction from that unit and from the other path. 3. There is no evidence that the motoneurone, following its discharge, remains refractory for a period longer than the absolute refractory period of the nerve fibre. On the contrary there is evidence to show that where afferent paths converge, a propagated disturbance arriving by one can take effect immediately the peripheral least interval after a previous excitation by the other has passed. During this interval there is some evidence that the afferent disturbance can be deferred in effect at the locus of convergence. REFERENCES. (1) Adrian, E. D., Joum. of Physiol., vol. 55, pp (1921). (2) Beritoff, J. S., *Zeitschr. f. Biol., vol. 62, pp (1913). (3) Briicke, E. Th., Zeitschr. f. Biol., vol. 76, pp (1922). (4) Briicke, E. Th., and F. Plattner, Akad. der Wissen. in Wien, Math.-naturw. Kl. Sitzungsb., vol. 131, Ab. I ll, pp (1923). (5) Buchanan, F., Proc. Physiol. Soc., pp. ii-iii; Joum. of Physiol., vol. 64 (1927-8). (6) Cooper, S., D. E. Denny-Brown, and C. S. Sherrington, Roy. Soc. Proc., B, vol. 100, pp (1926). (7) Cooper, S., D. E. Denny-Brown, and C. S. Sherrington, *Roy. Soc. Proc., B, vol 101, pp (1927). (8) Forbes, A., L. H. Ray, and F. R. Griffith, Amer. Joum. of Physiol., vol.. 66, pp (1923). (9) Gasser, H. S., and J. Erlanger, Amer. Joum. of Physiol., vol. 73, pp (1926). DESCRIPTION OF PLATE 13. All figures read from left to right and show simultaneous electrical and mechanical records of contraction. Time is shown by small vertical fines at the top of each figure at intervals of 0 02 sec. The onset and finish of the A stimulus are shown by the fall in the signal fines Sx and S2 respectively, similarly S3 and S4 mark the B stimulus. Between St and S3 stimulus A alone is causing discharge, and between S3 and S4 stimulus B alone causes discharge. Between S3 and Sa both stimulus A and stimulus B are active. The rate of the B stimulus is shown in the fine B traced by a magnetic signal in the stimulus circuit, and that of the A stimulus in the lower fine A when recorded. The tension scale
9 Coloured Globules in Retina o f Hen. 371 for figs. 1, 2 and 4 is given at the right-hand side of fig. 4, and that for figs. 3 and 5 at the right-hand side of fig. 3. Galvanometer string tension, 3-5 mm. for 1 m.v. i, Semitendinosus. Motor response from double stimulation of the intact motor nerve. Stimulus A, Berne coil, 10 cm., rate 49 a sec. Stimulus B, class coil, 5-5 cm., rate 46-5 a sec. Fig. 2. Semitendinosus. Reflex response. Stimulus A to peroneal nerve, 13 cm., rate 49 a sec. Stimulus B to popliteal nerve, 9-5 cm., rate 41-5 a sec. Fig. 3. Semitendinosus. Reflex response. Stimulus A to internal saphenous nerve, 10 cm., rate 51'5 a sec. Stimulus B to peroneal nerve, 7 cm., rate 47-5 a sec., K2H P 04 in distal lead. One complete beat between and x2. Fig. 4. Semitendinosus. Reflex response. Stimulus A to internal saphenous nerve, 10 cm., rate 49 a sec. Stimulus B to popliteal nerve, 8-5 cm., rate 47 a sec. After y the break shocks of the A stimulus begin to fall before each corresponding break shock of the B stimulus. Fig. 5. Semitendinosus. Reflex response. Stimulus A to peroneal nerve, 10 cm., rate 61 a sec. Stimulus B to nerve to quadriceps, 8 cm., rate 59*5 a sec. The complete beat of the stimulus series occurs between the two arrows The Absorption of Light by the Coloured Globides in the Retina of the Domestic Hen. By H. E. R o a f. (From the Department of Physiology, London Hospital Medical College.) (Communicated by Sir Charles Sherrington, F.R.S. Received July 30, 1929.) [Plate 14.] Schultze (1866) pointed out that the coloured globules* in the retinae of birds might afford a means whereby stimulation of the cones would be restricted to certain regions of the visible spectrum (7). A few other investigators have ascribed sensual discrimination of colour to retinal filters situate in front of the specific receptors for light (1, 4 and 6). An alternative view (2, 3) regards the coloured globules as decreasing, merely generally and relatively unselectively, i.e., quantitatively rather than qualitatively, the amount of light of short wave-length which reaches the sensitive (outer) limb of the cones. This might possibly be useful by reducing the amount * See figure in colours for the ben. Prenant, Bouin and Maillard, Traite d Histologie, vol. 1, p. 364, Paris, 1904.
10 hper and D enny-brown. Roy. Soc. Proc., B, L05, PI (Facing p* 370.)
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