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1 ON AN APPARENT MUSCULAR INHIBITION PRO- DUCED BY EXCITATION OF THE NINTH SPINAL NERVE OF THE FROG, WITH A NOTE ON THE WEDENSKY INHIBITION. BY V. J. WOOLLEY, Fellow of King's College, Cambridge. (From the Physiological Laboratory, Cambridge.) SINCE Wedenskyl first published his discovery of the effects of strong faradisation of the frog's sciatic, numerous observers have described the same results which he obtained, and from time to time some special case of his general law is put forward as a proof of the presence of inhibitory nerve fibres in the nerve trunks supplying the skeletal muscles. What Wedensky showed was that if the nerve of a muscle-nerve preparation was excited by an interrupted induced current, an apparent inhibition took place when the strength of the current or the rapidity of its interruptions was increased beyond a certain point. This effect was only noticeable when the muscle was slightly fatigued. The strong current moreover was not only unable itself to bring about a maximal muscular contraction, but also it rendered the whole nerve trunk inexcitable by any weaker stimulus. A stimulation so strong as to produce this inhibitory effect Wedensky named the "pessimum" stimulus in contradistinction to the weaker " optimum " stimulus which called forth a maximal contraction of the muscle. It follows from these resuilts that if a nerve is excited at one point continuously with an "optimum" stimulus, while a "pessimum" stimulus can be applied from time to time at another point, then every application of the latter will bring about an incomplete relaxation of the muscle. This experiment is the one which has been most frequently repeated in various forms by subsequent investigators. For instance Kaiser2 substituted a chemical stimulus for the optimum electrical one, 1 Pftuiger's Arch. xxxsvn. p Arch. de Physiol. norm. et path. s. 5, xii. p Zeitschr. f. Biol. xxvii. p PH, XXXVI. 12
2 178 V. J. WOOLLEY. and by strong faradisation of the upper end of the sciatic obtained an inhibition of the tetanus which was produced by applying glycerine to the middle of the nerve. During the current year Nicolaides and Dontas1 have published an account of an experiment which they regard as a demonstration of the inhibitory nerve fibres of skeletal muscle. They have shown that if a continuous tetanus of the frog's gastrocnemi-us is produced by a strong excitation of the eighth spinal nerve, then a weaker excitation of the ninth nerve will frequently bring about a relaxation. On this ground they contend that the ninth nerve contains inhibitory fibres to the gastrocnemius muscle. Now at first sight this phenomenon appears to differ materially fromn that which Wedensky discovered. For Nicolaides and Dontas apparently do not apply to the ninth nerve any stimulus other than that by which the inhibition is effected, whereas the Wedensky inhibition would be obtained only if a strong stimulus were sent into a nerve which was already excited by a weak one. Btut I think that the experiments which I propose to describe afford proof that the phenomenon described by Nicolaides and Dontas is in reality only another special case of Wedensky's general principle. For their phenomenon may be explained if we suppose that the ninth nerve is stimulated by the spread of current from the electrodes applied to the eighth, as well as by the current directly applied to it. The first point to which my experiments were directed was the obtaining with certainty the phenomenon- described. For Nicolaides and Dontas did not find the phenomenon constant in different frogs, perhaps because they always confined themselves too closely to the relative strengths of stimulus which they describe. Whatever its cause it is unlikely that in similar frogs it should be obtainable in one and ilot in another, and I found that by the following method it could be produced without fail. The lower root is excited with a coil in the ordinary way, the strength of the current being gradually increased from a subminimal to an optimal value. As soon as the curve has begun to fall slightly, a sudden increase in the strength of the current will produce a very obvious relaxation which will give place to a renewed contraction if the current is weakened. This is the ordinary Wedensky effect obtained with one root instead of with the nerve trunk, and it is with stimula- 1 Sitzungab. d. k. preuesischen Akad. p
3 INHIBITORY NERVES TO MUSCLE. 179 tions of this increased strength that the root in question will produce the inhibition which Nicolaides and Dontas have described. If we now apply the same method to the upper root, but, instead of stopping short at the "pessimum" point, increase the strength of the stimulating current still further, we obtain a second contraction, generally higher than the first one. It is a stimulation of this strength which must be used to obtain the tetanus which is to be inhibited by a "pessimum" stimulation of the other root, and the contraction which it causes is without doubt mainly due to a spread of the exciting current to the fibres coming fromn the other root. Having found a means of constantly obtaining the phenomenon, I applied it to the stimuilation of the eighth root which according to Nicolaides and Dontas does not give an inhibitory effect (though they suggest that in rare cases inhibitory fibres may be present in this root), and found that here also the inhibitory effect can be produced with equal constancy. The following tracing shows the inhibitory effect of exciting the upper root which according to Nicolaides and Dontas contains no inhibitory fibres. In this and all other tracings the time marker marks seconds and the curves must be read from right to left. Fig. 1. The lower root was stimulated throuighout by one coil, the distance between the coils being 103 mm., while the upper root was stimulated during the periods from A to B by another coil in which the distance between the coils was 140 mm. Each coil was driven by one Daniell cell. It will be seen that the relaxation while the latter current was applied was very nearly as great as the relaxation when all stimulation ceases at C.
4 180 V. J. WOOLLEY. That this result is not due to an abnormal distribution of the nerves in the animal used is shown by the tracing below. It was made immediately after the previous one with the same preparation, but in this case (as in the experiments of Nicolaides and Dontas) the tetanus is produced by stimulation of the upper root (coil 98) while the inhibition during the portions from A to B is caused by stimulation of the lower one (coil 93). As a general rule, however, it is not easy to demonstrate the phenomenon a second time with the roots reversed as in this case, because the strong currents required to produce a tetanus which is capable of being inhibited in this vay so injure the particular root used that it cannot be subsequently excited so as itself to produce the inhibition. Fig. 2. The explanation of the inhibition follows I think clearly from the method given above for its production. When such a strong current is applied to (for example) the eighth nerve, then all the nerve fibres which are directly stimulated will be paralysed and the muscle fibres which they supply will be practically relaxed. For the eighth nerve it is a "pessimum" stimulus, but for those fibres of the sciatic which proceed from the ninth nerve, and which are only stimulated by the spread of current from the eighth, it will be (if a suitable strength of current is employed) an optimum stimulus, which, like any other optimum stimulus, is capable of being inhibited by the "pessimum" stimulus which we proceed to apply to the ninth nerve by the other coil. To confirm this explanation of the facts observed I have applied cultents of similar strength to the peroneal branch of the sciatic, so causing, by spread of current, a tetanic contraction of the gastrocnemius. This tetanus may then easily be inhibited by the application
5 INHIBITORY NERVES TO MUSCLE. 181 of a " pessimum " stimulus to the sciatic trunk. In the tracing below, the tetanus was produced by stimulation of the peroneal nerve with the coil at 116 mm. and the relaxations from A to B in each case by stimulation of the sciatic (coil 112). Fig. 3. To avoid any danger of a reflex effect from the spinal cord the sciatic was cut through half-way down the thigh. Lest however there should be any nervous connection between the two nerves I have repeated the experiment, using a moist cotton thread in place of the peroneal nerve. In the following tracing such a thread was laid alongside the sciatic and " stimulated " by one coil (distance = 47) while the inhibitions from A to B were caused by stimulation of the sciatic by another coil (di-stance 170). This tracing shows particularly well the small teeth (Zacke) which Nicolaides and Dontas noticed in some of their curves during the inhibitory interval. They are probably due to some kind of interference between the two coils, as their frequency seems to depend on the ratio between the speeds of the two interrupters employed. Fig. 4.
6 182 V. J. WOOLLEY. I think that these experiments show clearly that the phenomenon in question is only another special case of Wedensky's original discovery. They also show the extreme care that is required in interpreting the results of stimulating the separate origins of nerve trunks or any short piece of nerve joining anotlher. Though the fact that stimulation of a branch of a nerve with currents of moderate strength can cause contractions in muscles not supplied by the branch is, of course, not new, I think that the possibilities of such sources of error have been underestimated by many observers. Note on the Wedensky inhibition. No completely satisfactory explanation of this phenomenon has been given. That it is not due to electrotonic changes in the nerve trunk-a view which has been suggested-is I think shown by the following experiment. The upper end of the sciatic is placed on a pair of non-polarisable electrodes, while the middle of the nerve can be excited by metallic electrodes connected with an ordinary coil. By the non-polarisable electrodes the upper end of the nerve could be excited by a rapidly made and broken battery-current given by the apparatus described below (cp. Fig. 5). Fig. 5. A, B, C and D are brass plates, eight rectangular and eight wedgeshaped, let into the surface of a fibre cylinder. Each plate is electrically connected to an insulated metal ring (A', B', C', D') around the axis on which the whole revolves. Contacts are made on each ring and on the metal plates by six brushes not shown in the sketch. The brushes in contact with the plates are connected with the nerve and the other brushes with a battery. Thus, if the rings A' and B' are connected with one pole and C' and if with the other, eight brief currents will be passed through the nerve in each revolution, all the currents being in the same direction. If on the other hand A' and D' are connected with one pole and B' and C with the other, then the eight currents will be passed through the nerve alternately in opposite directions. By moving
7 INHIBITORY NERVES TO MUSCLE. 183 the brush in contact with the wedge-shaped plates C and D currents of varying duration may be employed. A counter is arranged to make a contact every hundred revolutions. With this apparatus it is easy to prove that a powerful inhibition may be obtained by the application of a current made and broken with sufficient frequency, while the same current if acting constantly upon the nerve is without any visible effect. In the tracing given in Fig. 6 the two tetanic contractions of the gastrocnemius registered were produced by faradisation of the sciatic by the metallic electrodes applied to the middle of the nerve. During the first (right hand) tetanus a constant descending current, of E.M.F. *25 of a Daniell, was passed through the upper end of the nerve during the time marked by the depression of the signal. During the second tetanus a current of the same strength and in the same direction was applied, but was interrupted at a rate of about 200 times per second. It lasted for the period marked A to B on the curve, and produced the well-marked inhibition shown. The two depressions of the signal in -U- Fig. 6. the second tetanus show the time occupied by a hundred revolutions of the interrupter, and do not mark the application of the stimulus. In this experiment the interrupter was so arranged that the period during which the current was closed was equal to that during which it was open. The experiment shows clearly that the inhibitory effect which Wedensky discovered cannot possibly be due to electrotonus.
8 184 V. J. WOOLLEY. SUMMARY. 1. The inhibition which Nicolaides and Dontas obtain by stimulation of the ninth spinal nerve of the frog can equally well be obtained by stimulation of the eighth. 2. In either case the nerve fibres of the root which appears to cause the contraction are in reality paralysed by the strong current used as in the well-known Wedensky effect. The contraction is actually due to a spread of current to the fibres of the other root, which in their turn are more or less paralysed by the additional stimulus applied to them, thus simulating a direct inhibition. 3. That this is the source of the contraction is shown by the fact that currents of the strength necessary to bring about a contraction to be so inhibited, when applied to the peroneal branch of the excised sciatic, cause a powerful contraction of the attached gastrocnemius. 4. That the Wedensky inhibition cannot be due to electrotonic action of the strongr currents employed is shown by the fact,that a constant current which is unable to affect the result of a tetanising stimulus applied to another part of the nerve will nevertheless bring about a marked inhibition if it is sufficiently frequently interrupted.
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