Search

The observations with which the present communication deals were met with in experiments continuing those on reciprocal innervation of symmetrical muscles. In my previous paper on that subject it had been reported that in regard to symmetrical extensors of the knee the ratio borne by intensity of the ipsilateral inhibition to the contralateral excitation is such that with equal stimuli to right and left symmetrical afferent nerves there is inhibitory suppression of contraction in both the muscles. In other words, under double reciprocal innervation the ipsilateral inhibition by each nerve completely overcomes the contralateral excitation of the other. It was shown that this mutual suppression holds over a wide range of the scale of intensities of stimulation. It was also shown that with quite weak stimuli a simultaneous stimulation of both nerves, stimuli being equal in intensity, often results in concurrent contraction of both muscles. Indeed, with quite weak stimuli, the effect of stimulation of each afferent nerve by itself is, in the decerebrate preparation, usually contraction of the ipsilateral as well as of the contralateral muscle. This being so, it is evident that at some point in the scale of intensities of stimulation there should be a place below which contralateral excitation is stronger than ipsilateral inhibition, whereas above it ipsilateral inhibition is stronger than contralateral excitation.

I. Reflex excitation and inhibition when brought to play simultaneously on the motoneurones of an extensor muscle can be so balanced that there results in the muscle a contraction , the degree of which evidences algebraic summation is obtainable not only in the decerebrate animal but also in the purely spinal, for instance, after decapitaion. This circumstance much facilitates the physiological study of the phenomenon. In other words, the grading (fig.1) of reflex contraction of the extensor by varying intensity of inhibition acting along with reflex excitation can be studied in the animal freshly made spinal as well as in the animal in the decerebrate condition. The muscle which I have chiefly employed in the purely spinal preparation is the isolated extensor of the knee in the decapitated cat. A difference does indeed exist between the reactions of the preparation in the decapitated and in the decerebrate condition. In the decapitated preparation, as in the decerebrate, the reflex effect of any inhibitory afferent is easily seen if stimulation of that afferent is employed concurrently with stimulation of an excitatory afferent. If however the inhibitory afferent is stimulated during the ordinary resting condition of the preparation, there is usually no change in the muscle to show that the inhibitory afferent is producing any effect at all (fig. 2). This is because the extensor muscle in the decapitated preparation is not exhibiting tonus and lies relaxed, therefore affording no background of contraction against which an inhibitory reflex can reveal itself by causing relaxation. Even in this condition it can, however, easily be shown that the inhibitory afferent is then really producing a state of inhibition in the preparation, although that state is not made evident by any further relaxation. If a stimulus sufficient to cause reflex contraction of the muscle be applied to the excitatory afferent while the inhibitory afferent, although apparently without effect, is being stimulated, the excitatory afferent is found to be ineffective (or only partially effective) then; but it, immediately becomes effective (or more effective) on withdrawal of the concurrent inhibitory stimulation (fig. 2).

In further prosecution of observations made in Ludwig’s laboratory by Schmiedeberg and by Bowditch, N. Baxt in 1875 carried out in that laboratory a prolonged enquiry into the effect produced on the heart’s frequence by combined stimulation of the inhibitory ( vagus ) and accelerator ( accelerans ) nerves going to that organ. His observations were made on large dogs; the two nerves were faradised simultaneously. In most of his experiments, stimulation of accelerans preceded that of vagus by a few seconds, to allow for the well-known longer latency of the former’s reaction; the precurrent stimulation of accelerans alone was immediately followed by stimulation of both nerves simultaneously. Baxt found the rate of heart-beat under the combined stimulation slowed as though the vagus only and no accelerator was in operation; but, immediately following on cessation of the combined stimulation, a full accelerator effect appeared, as though no stimulation of the vagus had taken place. Baxt employed usually minimal stimulation of vagus and maximal of accelerans , for he found minimal excitation of vagus suffice to set aside completely, for the time being, maximal excitation of accelerans . In his hands, the result of the combined stimulation was vagus action, even when weakest, completely obscuring accelerans action even at strongest; but although the accelerans action showed no trace of its existence during the vagus stimulation, it appeared in full force after the vagus action had passed off. The vagus action, therefore, did not destroy it, but merely postponed its appearing. Baxt drew the conclusion that the inhibitory nerve and the excitatory nerve must act on separate points in the heart’s mechanism and are not true antagonists. This view has since been endorsed by many, but is not that of v. Cyon, the discoverer of the accelerator . Another field for examination of the same problem was chosen by v. Frey. He investigated the effect on the venous flow from the sub-maxillary gland of simultaneous stimulation of the vaso-constrictor ( cervical sympathetic ) and the vaso-dilatator ( chorda tympani ) nerves. The dilatating influence of the chorda proved to be completely overpowered by the constricting effect of the sympathetic during combined stimulation of the two. But on discontinuing the combined stimulation there ensued from the vein a markedly excessive blood-flow, i. e ., a marked chorda action ensued as an after-effect. The action of the sympathetic had, therefore, not destroyed the action of the concurrently excited chorda, it had only postponed its appearing, v. Frey, with his customary clearness, wrote: “the antagonism between constrictor and dilatator has not as its basis a simple summing of two forces which act in opposite direction at the same point of application.” The sympathetic prevails entirely for the time being as regards the surface effect, but the chorda nevertheless develops with regular course the change characteristic of its action, and does so “in some part of the excitable apparatus protected from the attack of the sympathetic: only in some other place do the actions of the two collide.”

The following two reactions, observable in the extensor muscle of the knee, appear not without importance for the reflex co-ordination of antagonistic movements at that joint. They are reactions favourably studied in decerebrate rigidity. The cat is the animal in which, under that condition, my results have been chiefly obtained. The reactions can be observed as follows:—In the decerebrate animal a preparation of the extensor of the knee is so made that by detachment of other muscles, or severance of other nerves, the vasto-crureus muscle, with its nerve-branch from the anterior crural trunk, remains the sole nerve-muscle component intact in the whole limb. The vasto-crureus is one of those muscles which, after decerebration, exhibits the marked tonus characteristic of decerebrate rigidity. This tonus of the vasto-crureus then maintains the knee in an attitude of partial or complete extension. The flexor muscles of the knee, together with all the other muscles acting on that joint, have been paralysed by section of their nerves.

It was shown in previous notes of this series that in the “flexion-reflex” of the limb the reflex inhibition of the extensor muscles is frequently followed by contraction of them. This contraction ensues immediately on cessation of the inhibitory stimulus, and is often more accentuated than was the contraction originally inhibited. The phenomenon was ascribed to a process of rebound in the central of the nervous are inhibited, and this process, on account of its seeming analogy with certain visual phenomena often called “inductive,” was termed “successive induction.” The occurrence of this “successive induction” made it seem probable that under favourable conditions the reflex evoked in the limb by a single stimulus would be diphasic with a first phase of flexion followed by a subsequent phase of extension. The following observations show that this is in fact the case, and under appropriate conditions regularly so.

I. In previous notes on this subject the examples of reciprocal innervation taken from the limb muscles have usually been from muscles acting at the knee. An advantage offered there is that the vasti and crureus , extensors of the knee, act directly on that one joint alone. A muscle acting on two joints is often an extensor of one of the joints and a flexor of the others. When such a muscle is thrown into contraction by reflex action, there may be a dilemma as to whether it is as an extensor or as a flextor, that it is acting, and the answer will depend partly on the kind is gastrocnemius ; it extends the ankle and flexes the knee. It is, therefore, of interest to examine how this muscle behaves when its antagonist, tibialis anticus , a flexor of the ankle, is thrown into contraction by reflex action. Stimulation of any among various points of skin, or of the proximal end of various afferent nerves of the leg, excites reflex contraction of tibialis anticus. A nerve often used for the purpose in my observation has been the cutaneous branch of the peroneal nerve about a centimetre above the ankle (cat). In the reflex which then occurs in the limb, the following points can be made out. The ankle is flexed, and with the flexion of ankle occurs also flexion at knee and hip. If the anterior crural, obturator, hamstring, and popliteal nerve trunks, the insertions of iliopsoas, and psoas parvus, and the origin of pectineus muscles be severed, active flexion of knee and hip are excluded from the reflex. The active flexion at ankle still persists. On inspecting the tendons of the pretibial flexors of the ankle, that of tibialis anticus is seen to be drawn upward at each reflex, and with it also those of extensor longus digitorum and peroneus longus, but in my experience these latter are retracted less. If, in addition to the nerves and muscles mentioned above as severed, but the branch from the popliteal nerve to the gastrocnemius be spared, and that muscle be exposed to inspection, usually no change in that muscle appears.

If we attempt to decipher the biological meaning of reciprocal innervation its various instances when marshalled together say plainly that one of the functional problems which it meets and solves is mechanical antagonism. Where two muscles have directly opposed effect on the same lever, “reciprocal innervation” is the general rule observed by the nervous system in dealing with them, and this holds whether the reciprocal innervation is peripheral as with the antagonists of the arthropod claw, or is central as with vertebrate skeletal muscles. Also where one and the same muscle is governed by two nerves influencing it oppositely, reciprocal innervation seems again the principle followed in the co-ordination of the two opponent centres, as has been shown by Bayliss in his observations on vasomotor reflexes. But the distribution and occurrence of reciprocal innervation extend beyond cases of mere mechanical antagonism. The reflex influence exerted by the limb-afferents on symmetrical muscle-pairs such as right knee-extensor and left is reciprocal. Thus right peroneal nerve excites the motoneurones of left vastocrureus, and concomitantly inhibits those of the right. The reflex inhibition of the one is concurrent with, increases with increase, and decreases with decrease of, the excitatory effect on the other. Here the muscles are not in any ordinary sense antagonistic; not only do they not operate on the same lever, but they are not even members of the same limb, nor do they belong even to the same half of the body. They are, however, actuated conversely in the most usual modes of progression—the walking and the running step—though not always in galloping.

In a paper published in the year 1893, after describing various experimental results on vascular reflexes, I made use of the following words: “the simplest explanation of the above results is the depressor nerve acting in an inhibitory manner on the former, and in an exciting manner on the latter, while pressor nerves act in an opposite way on both.” The evidence brought forward at that time in support of this view was mainly indirect, and in no way comparable with the brilliant experimental proofs afforded by Sherrington’s masterly researches on the similar phenomena in the case of the reflexes to voluntary muscles. These latter results have, however, given renewed interest to the question, and the following pages contain an investigation whose object was to obtain direct experimental evidence whether or not the phenomena of vascular reflexes can be brought into line with those affecting skeletal muscle.