The Integrative Action of the Nervous System

the two arcs respectively" (Fig. 55). "When a strong stim- ulus is applied to the afferent neurone of arc a it generates neurin rapidly, so that it becomes very rapidly charged, and the resistance of synapse a-^ — a^ is lowered until a series of dis- charges takes place from a^ to ^g* ^"^ again from a^ to a^. The problem is, then, to imagine such a mode of connection between arc a and arc b as will cause arc a during stimulation to drain off from the afferent and central neurones of b the smaller quantities of neurin generated in them. Several forms of such a connection may be imagined, but I think that probably it takes the form of a collateral fibre coming from neurone b^, and taking part with the axone of a^ in forming a synapse with ^3." " Whatever the exact constitution of this synapse may be, we may assume that, when its resistance is lowered by the stimulation of a^ and con- sequent charging of a^y the collateral of ^2> making connection with a^, through this synapse, becomes the path of least resist- ance for the escape of neurin from b^ and ^2- These neurones are therefore drained by a^, while b^ ceases to receive any neurin from ^2» 2i"d the tone of the muscle-group supplied by it is abolished." " In a similar way, if both a^ and b^ be stimulated, but one more strongly than the other, the more strongly stimu- lated arc will drain the afferent and central neurones of the less strongly stimulated arc, because the resistance of synapses of the former will be reduced to a lower level than that of the synapses of the latter." This scheme fits a number of facts of reciprocal inhibition.

Thus, in reciprocal innervation, as the term itself implies, the inhibition at one part always appears as the negative aspect of positive excitation at another. To " alternating " reflexes, which are common as spinal reactions, Macdougall applies the scheme thus : " We must suppose the collateral connection of the arc a (to which we may suppose the stimulus to be applied) with the neurone b^ to be but little inferior in conducting capacity to its direct connection with a^. When, then, the neurone a is stimulated continuously, the arc will first discharge into a^ and drain b-^ and b^ (J. e. inhibit ^3) until after some little time fatigue causes the resistance of synapse a^ — a^ to become slightly greater than that of synapse b,^ — ^3, when a^ will discharge with ^2 wholly into ^3, and a^ will be in turn "inhibited." So the charges of the afferent neurones of both arcs will be dis- charged into ^3 until fatigue causes rise of resistance of the synapse on ^3." The high influence of intensity of reaction in determining whether the reaction shall or shall not replace another reaction is expressed by this scheme very lucidly. Also the occurrence under strychnine^^ and tetanus toxin of excita- tion at a synapse where inhibition is otherwise the rule seems a contingency which the view answers well. If these agents (strychnine presumably from the afferent side, tetanus toxin from the efferent) reduce the resistance at synapse a^ — ^3, there will, on stimulation of a-^^ be conversion of the inhibition of b^ in excitation, just as in the second phase of an alternating reflex, but the resistance at synapse a^ — a^ not being raised, as it is in the second phase of the alternating reflex, a^ will also be excited as usual, and both antagonistic muscles will contract, as I have shown they do in fact in strychnine reflexes and as they do in the convulsions of strychnine poisoning.

The scheme makes it clear, too, that this double discharge, or leakage, will prove rapidly exhausting on the central arcs, and indeed the phasic character of the attacks in strychnine poisoning does seem due to rapid exhaustion following each convulsive discharge. Again, in working with tetanus toxin, I have,^^ in the gradual progress of the disease, several times found the afferent nerves produce a slight reflex inhibition of the extensor of the

:nee, if the initial posture at the knee were at the time exten- jion (/*. e.y the extensor arc in high activity), and yet produce listinct excitation of the extensor if the initial posture at the ime were flexion (/. e.y the extensor arc in less activity). These jffects of strychnine and tetanus toxin the view of Macdougall jeems well fitted to meet, though they were not known at the ime the view was formulated. The view seems also applicable some of the results obtained in the interesting experiments )y V. Uexkiill on Invertebrata.

One difficulty however seems to me presented by Macdougall's lew, and it is that the diversion of the influence of a^ through ►2 away from a^ which constitutes inhibition does not suggest reason for the superactivity (successive induction) in a conse- [uent on the inhibition. And a more serious difficulty, attaches, in my thinking, to the view, — at least, as it at present stands — in that it seems to sever this central nervous inhibition — of which I regard reciprocal innervation of antagonistic muscles as

met peripherally in the heart, blood-vessels, and viscera, rather than to connect it with them. It appears to me unlikely that in their essential nature all forms of inhibition can be anything but Another important class of sequence of antagonistic reflexes is that which gives the " compensatory reflex." A compensa- tory reflex occurs where the reflex is a return to a state of reflex equilibrium which had been disturbed by an intercurrent reflex to which the compensatory reflex is the diametrical antagonist Some compensatory reflexes are excited by passive movements, others by active movements. It is the latter which come under consideration here. Many reflex movements are intercurrent reactions, breaking in on a condition of neural equilibrium itself reflex. Take the case of the flexion-reflex of the leg (spinal dog) induced by a brief stimulus during " decerebrate rigidity," where the animal may be regarded as a bulbo-spinal machine. Sup- pose the animal suspended with spine horizontal and limbs pendent. The limbs are then in slight active extension, much

as if the animal were standing. This slight extension is active, for it is reflex, and the peripheral source of the maintained re- flex pose is traceable to arcs arising in the extensor muscles, in alliance probably with some from the otic labyrinth. The crea- ture breathes quietly and regularly. Its skeletal musculature otherwise exhibits no movements, although its reflex activity is considerable and in progress all the time, as shown by the steady reflex extension of the limbs. If, then, the foot be excited by a brief stimulus and thus a flexion-reflex induced in the limb, the limb is drawn up at hip, knee, and ankle. The movement is brief; after being drawn up, the limb returns to its previous pendent posture. It is easy in many instances to perceive that the pose of extension, as resumed, is more marked than it was prior to the intercurrent reflex or flexion. It is also equally easy to perceive that in the replacement of the limb the exten- sion is not a mere passive drop under gravity, but is a rever- sion to the previous posture by an active movement In such a case the reflex effect of the intercurrent stimulus seems to cease with the cessation of the intercurrent reflex (flexion) which the stimulus immediately provoked. But closer examina- tion shows that this is not really the case. There is an active reflex return to the pre-existing pose. Thus, the disturbing stimulus brought about not only the flexion-reflex, but, second- arily to that, a reflex antagonistic to that. This latter antago- nistic (extension) reflex is " allied " to that which originally held the field. When the flexion-reflex disturbed the neural equi- librium it dispossessed the opposed reflex of extension from certain final paths common to that and itself.

In other words, its own reaction induces an after-coming reflex antagonistic to itself, and this brings resumption of the original reflex attitude that, under the condition (gravity, etc.) obtaining at the time, satisfies neural equilibrium. The whole intercurrent reflex dis- turbance is really ended by a "compensatory reflex." The compensatory reflex in this case seems traceable primarily to proprio-ceptive (muscular) aflerents fi-om the muscles, joints, etc., of the limb. But compensatory reflexes are particularly evident in reflex reactions started by labyrinthine affe rents

(Ewald, Lee, Loeb, Lyon, Muskens, Nagel, and others), and in the decerebrate animal this compensatory reflex of the limb is presumably due to muscular afferents of the limbs and to labyrinthine afferents acting in reflex alliance. Among the afferent nerves of importance to this compensat- ing reflex there seems particularly that of the vasto-crureus muscle itself, the extensor of the knee. Electrical stimulation of the central end of that nerve excites contraction of the flexors of hip and knee and inhibits the vasto-crureus itself. It therefore reinforces the flexion-reflex, but its stimulation is, on being dis- continued, immediately succeeded by contraction of the extensorf i muscles. This rebound (successive induction) is particularly''- marked in the vasto-crureus itself. These instances exemplify, further what was said as to the close connection of secondary, not immediate, kind between reflexes initiated by receptors of the extero-ceptive {e.g. skin) surface and reflexes initiated by receptors of the deep, i. e, proprio-ceptive field. But in the instances given earlier the proprio-ceptive reflex which was initiated secondarily in consequence of the foregoing extero- ceptive (skin) reflex is antagonistic to the latter; the two reflexes are related as antagonistic reflexes.

The secondary association which, as pointed out earlier, holds so generally be- tween certain extero-ceptive proprio-ceptive pairs of reflexes and connects them, forms some of its pairs from " allied re- flexes " and others from " antagonistic reflexes." In the former case the coupling is " simultaneous," in the latter ** successive." Proprio-ceptive reflexes may themselves be coupled in antago- nistic pairs ; of this, one example is the reflex contraction of the hamstring muscles, which sometimes undoubtedly ensues on stim- ulation of the central end of the nerve of the extensor of the knee (I was at first inclined to attribute this to escape of current, but am convinced it occurs truly reflexly sometimes) ; and another example is Mislawski's and Baglioni's interesting expiratory reflex elicitable from the afferent fibres of the phrenic nerve.

Factors determining the sequence. The formation of a com- mon path from tributary converging afferent arcs is important because it gives a co-ordinating mechanism. There the domi- nant action of one afferent arc, or set of allied arcs in condomin- ium, is subject to supercession by another afferent arc or set of allied arcs, and the supercession normally occurs without inter- current confusion. Whatever be the nature of the physiological process occurring between the competing reflexes for dominance over the common path, the issue of their competition, namely, the determination of which one of the competing arcs shall for the time being reign over the common path, is largely condi- tioned by four factors. These are " spinal induction," ^^ rela- tive intensity of stimulus, relative fatigue, and the functional species of the reflex.

I. Spinal induction. The first of these occurs in two forms, one of which has been already considered, namely, ** immediate induction." It is a form of " bahnung." The stimulus which excites a reflex tends by central spread to facilitate and lower the threshold for reflexes allied to that which it particularly excites. A constellation of reflexes thus tends to be formed which reinforce each other, so that the reflex is supported by allied accessory reflexes, or if the prepotent stimulus shifts, allied arcs are by the induction particularly prepared to be responsive to it or to a similar stimulus.

Immediate induction only occurs between allied reflexes. Its tendency in the competition between afferent arcs is to fortify the reflex just established, or, if transition occur, to favour transi- tion to an allied reflex. Immediate induction seen;is to obtain with highest intensity at the outset of a reflex, or at least near its commencement. It does not appear to persist long. The other form of spinal induction is what may be termed successive induction. It is in several ways the reverse of the preceding.^^

In peripheral inhibition exemplified by the vagus action on the heart the inhibitory effect is followed by a rebound after- effect opposite to the inhibitory (Gaskell). The same thing is obvious in various instances of the reciprocal inhibition of the spinal centres. Thus, if the crossed-extension reflex of the limb of the spinal dog be elicited at regular intervals. say once a minute, by a carefully adjusted electrical stimulus \ of defined duration and intensity, the resulting reflex move- 1

acter, amplitude, and duration. If in one of the intervals i a strong prolonged (e. g. 30") flexion-reflex is induced from 1 the limb yielding the extensor-reflex movement, the latter -■ reflex is found intensified after the intercurrent flexion-reflex.*^ > The intercalated flexion-reflex lowers the threshold for the - aftercoming extension-reflexes, and especially increases their \ gressively diminishing, through four or five minutes, as tested i

by the extensor-reflexes at successive intervals. Now, as we ;] have seen, durifig the flexion-reflex the extensor arcs were 1 inhibited: after the flexion-reflex these arcs are in this case \ evidently in a phase of exalted excitability. The phenomenon | presents obvious analogy to visual contrast. If visual bright- \ ness be regarded as analogous to the activity of spinal dis- '\ charge, and . visual darkness analogous to absence of spinal J discharge, this reciprocal spinal action in the example men- %

tioned has a close counterpart in the well-known experiment ■ where a white disc used as a prolonged stimulus leaves as visual ^ after-effect a gray image surrounded by a bright ring (Hering's \ ** Lichthof "). The bright ring has for its spinal equivalent the ; discharge from the adjacent reciprocally correlated spinal centre. The exaltation after-effect may ensue with such intensity that : simple discontinuance of the stimulus maintaining one reflex is \

antagonistic reflex. Thus the " flexion-reflex " if intense and i prolonged may, directly its own exciting stimulus is discontinued, ; be succeeded by a " spontaneous " reflex of extension, and this even when the animal is lying on its side and the limb hori- \ zontal, — a pose that does not favour the tonus of the extensor \ muscles. Such a " spontaneous " reflex is the spinal counter- \ part of the visual ** Lichthof." To this " spinal induction," as i

it may be termed, seems attributable a phenomenon commonly : met in a flexion-reflex of high intensity when maintained by very \ prolonged excitation. The reflex-flexion is then frequently ' Figure 58. — The crossed extension-reflex. This reflex was being elicited regularly by eleven break shocks (unipolar faradization to skin of opposite foot) at one-minute inter- vals, stimulus and reflex being of low intensity. In the interval between B and C a strong flexion-reflex of the limb responding in the crossed extension-reflex was provoked and maintained for 45 seconds. The next following extension-reflex C shows augmenta- tion; this augmentation is also evident, though less in the next crossed reflex D. In E, a minute later, the augmentation is seen to have passed ofif. The sigjnal recording the stimulation evoking each crossed extension-reflex is above. Time is marked in seconds below.

broken at irregular intervals by sudden extension movements (Figs. 45, 61). It would seem, therefore, that some process in the flexion-reflex leads to exaltation of the activity of the arcs of the opposed extension-reflex. And electrical stimula- tion of the proximal end of the severed nerve of the extensor muscles of the knee (cat), though it does not in my expe- rience directly excite contraction of the extensors of the knee, is on cessation often immediately followed by contraction of them.

Figure 59. — "Mark-time" reflex arrested by inhibition. Record of movement of limb (spinal dog). The upstrokes correspond with flexions. The reflex is interrupted by stimulation of the tail. This arrest is followed, after discontinuance of the inhibitory stimulus, by increased amplitude and some quickening of the leg-movement. Signal line marks duration of inhibitory stimulus. Time above in seconds. Figure 6o. — "Mark-time" reflex arrested by removing the exciting stimulus. Record of movements as before. During the period between the two marks on the signal line the reflex was interrupted by lifting the fellow-limb to that yielding the tracing. On letting the leg hang again, the reflex starts afresh, but without increase beyond its previous activity.

As examples of the rebound exaltation following on inhibi- tion the following may also serve.^^ The so-called *' mark-time " reflex of the " spinal " dog is an alternating stepping movement of the hind limbs which occurs on holding the animal up so that its limbs hang pendent. It can be inhibited by stimulating the skin of the tail. On cessation of that stimulus the stepping movement sets in more vigorously and at quicker rate than before (Fig. 59). The increase is chiefly in the amplitude of the movement, but I have also seen the rhythm quickened even by 30 per cent of the frequence.

This after-increase might be explicable in either of two ways. It might be due to the mere repose of the reflex centre, the re- pose so recruiting the centre as to strengthen its subsequent action. But a similar period of repose obtained by simply supporting one limb — which causes cessation of the reflex in both limbs, the stimulus being stretch of the hip-flexors under gravity — is not followed by after-increase of the reflex (Fig. 60). Or the after-increase might result from the inhibition being followed by a rebound to superactivity. This latter seems to be the case. The after-increase occurs even when both hind limbs are passively lifted from below during the whole duration of the inhibitory stimulus applied to the tail. It is the depres- sion of inhibition and not the mere freedom from an exciting stimulus that induces a later superactivity. And the reflex in- hibition of the knee-extensor by stimulation of the central end of its own nerve is especially followed by marked rebound to superactivity of the extensor itself.

Again, the knee-jerk, after being inhibited by stimulation of the hamstring nerve, returns, and is then more brisk than before the inhibition (Fig. 29, p. 89). ' By virtue of this spinal contrast, therefore, the extension- reflex predisposes to and may actually induce a flexion- reflex, and conversely the flexion-reflex predisposes to and may actually induce an extension-reflex. This process is qualified to play a part in linking reflexes together in a co- ordinate sequence of successive combination.^ If a reflex-arc A during its own activity temporarily checks that of an opposed reflex-arc B, but as a subsequent result induces in arc B a phase of greater excitability and capacity for discharge, it predisposes the spinal organ for a second reflex opposite in character to its own in immediate succession to itself. I have elsewhere ^^ pointed out the peculiar prominence of ** alternating reflexes " in prolonged spinal reactions. It is significant that they are usually cut short with ease by mere passive mechanical inter- ruption of the alternating movement in progress. It seems that each step of the reflex movement tends to excite by spinal induction the step next succeeding itself.

Much of the reflex action of the limb that can be studied in the " spinal " dog bears the character of adaptation to locomo- tion. This has been shown recently with particular clearness by the observations of Phillipson. In describing the extensor thrust of the limb I drew attention at the time to its signifi- cance for locomotion. " Spinal induction " obviously tends to connect to this extensor-thrust flexion of the limb as an after-effect. In the stepping of the limb the flexion that raises the foot and carries it clear of the ground prepares the antago- nistic arcs of extension, and, so to say, sensitizes them to respond later in their turn by the supporting and propulsive extension of the limb necessary for progression. In such reflex sequences an antecedent reflex would thus not only be the means of bringing about an ensuing stimulus for the next reflex, but would predispose the arc of the next reflex to react to the stimulus when it arrives, or even induce the reflex without ex- ternal stimulus. The reflex "stepping" of the "spinal" dog does go on even without an external skin stimulus : it will con- tinue when the dog is held in the air. The cat walks well when anaesthetic in the soles of all four feet.

Each reflex movement must of itself generate stimuli to afferent apparatus in many parts and organs — muscles, joints, tendons, etc. This probably reinforces the reflex in progress. The reflex obtainable by stimulation of the afferent nerve of the flexor muscles of the knee excites those muscles to contraction and inhibits their antagonistics : the reflex obtainable from the afferent nerve of the extensor muscles of the knee excites the flexors and inhibits their antagonists.

Where a reflex by spinal induction tends to eventually bring about the opposed reflex, the process of spinal induction is therefore probably reinforced by the operation of any reflex generated in the movement. This would help to explain how it is that a reflex reaction, when once excited in a spinal animal, ceases on cessation of the stimulus as quickly as it generally does. Such a reaction must generate in its progress a number of further stimuli and throw up a shower of centripetal im- pulses from the moving muscles and joints into the spinal cord. Squeezing of muscles and stimulation of their afferent nerves and those of joints, etc., elicit reflexes. The primary reflex movement might be expected, therefore, of itself to ini- tiate further reflex movement, and that secondarily to initiate

further still, and so on. Yet on cessation of the external stimulus to the foot in the " flexion-reflex " the whole reflex comes usually at once to an end. The *' scratch-reflex," even when violently- provoked, ceases usually within two seconds of the discontinu- ance of the external stimulus that provoked it. We have as yet no satisfactory explanation of this. But we remember that such reflexes are intercurrent reactions breaking in on a condition of neural equilibrium itself reflex. The suc- cessive induction will tend to induce a compensatory reflex, which brings the moving parts back again to the original posi- tion of equilibrium.

II. Fatigue. Another condition influencing the issue of com- petition between reflexes of different source for possession of one and the same final common path is " fatigue." ^^ A spinal reflex under continuous excitation or frequent repetition be- comes weaker, and may cease altogether. This decline is pro- gressive, and takes place earlier in some kinds of reflexes than it does in others. In the spinal dog the scratch-reflex under ordinary circumstances tires much more rapidly (Fig. 45) than does the " flexion-reflex."

A reflex as it tires shows other changes besides decline in amplitude of contraction. Thus, in the " flexion-reflex " the original steadiness of the contraction decreases (Figs. 45, 61); it becomes tremulous, and the tremor becomes progressively more marked aud more irregular. The rhythm of the tremor in my observations has often been about 10 per second. Then phases of greater tremor tend to alternate with phases of im- proved contraction as indicated by some regain of original ex- tent of flexion of limb and diminished tremor. Apart from these partial evanescent recoveries the decline is progressive. Later, the stimulation being maintained all the time, brief periods of something like complete intermission of the reflex appear, and even of a replacement of flexion by extension. These lapses are recovered from, but tend to recur more and more. Finally, an irregular phasic tremor of the muscles is all that remains. It is not the flexor muscles themselves which tire out, for these, when under fatigue of the " flexion-reflex " they contract no