The Integrative Action of the Nervous System

If in a monkey or cat transection below or in the lower half of the bulb has been performed, the animal when suspended, artificial respiration if necessary being kept up, hangs from the suspension points with deeply drooped neck, deeply drooped tail, and its pendent limbs flaccid and slightly flexed. The fore limb is slightly flexed at shoulder, at elbow, and very slightly at wrist. The hind limb is slightly flexed at hip, at knee, and at ankle. On giving the hand or foot a push forward and then releasing it, the limb swings back into and somewhat beyond the position of its equilibrium under gravity; and it oscillates a few times backward and forward before finally settling down to its original position.

To this condition of flaccid paralysis supervening upon tran- section in the lower half of the bulb the condition ensuing on removal of the cerebral hemispheres offers a great contrast. In the latter case the animal, on being suspended just as after the former operation, hangs with its fore limbs thrust backward, with retraction at shoulder joint, straightened elbow, and some flexion at wrist. The hand of the monkey is turned with its palmar face somewhat inward. The hind limbs are similarly straight- ened and thrust backward ; the hip is extended, the knee very stiffly extended, and the ankle somewhat extended. The tail in spite of its own weight, and it is quite heavy in some species of monkey, is kept either straight and horizontal or often stiffly curved upward. There is a little opisthotonus of the lumbo- sacral vertebral region. The head is kept lifted against gravity and the chin is tilted upward under the retraction and backward rotation of the skull on the neck. The mouth is kept closed and there is some stiffness in the elevators of the jaw. When the limbs or tail or head or jaw are pushed from the pose they have assumed considerable resistance to the movement is felt, and unHke the condition after bulbar section, on being released they spring back at once to their former position and remain there for a time more rigid than before.

The rigidity is immediately due to prolonged spasm of cer- tain groups of voluntary muscles. The chief of these are the retractor muscles of the head and neck, the elevators of the jaw and tail, and the extensor muscles of the elbow and knee, and shoulder {i,e, deltoids) and hip. In the dog and cat, just as spinal shock is more severe in the fore limbs than in the hind, so decerebrate rigidity is more marked in the fore than in the hind limb. This prolonged spasm may be maintained, with intermissions, for a period of four days. It is increased, and even when absent or very slight, may be soon developed by passive movements of the part. There is no obvious tremor in the spasm in the earlier hours of its continuance; later it does sometimes become tremulant.

Administration of chloroform and ether, if carried far, quite abolishes the rigidity. On interrupting the administration the rigidity again rapidly returns. Section of the dorsal columns of the spinal cord does not\ abolish the rigidity. Section of one lateral column of the cord in the upper lumbar region abolishes the rigidity in the hind limb of the same side as the section. Section of one ventro- lateral column of the cord in the cervical region destroys the rigidity in the fore and hind limbs of the same side.

The rigidity develops either very imperfectly or not at all in a limb the afferent roots of which have been severed some days prior to carrying out the operation which produces the rigidity. If after ablation of both cerebral hemispheres, even when the rigidity is being maintained at its extreme height, the affer- ent roots previously laid bare and prepared, are carefully severed, the limb at once falls flaccid. The result is quite local, that is, confined to the one limb the afferent roots of which are severed.

Decerebrate rigidity exhibits reflex excitation in those very groups of muscles which the local reflexes and the motor cortex when stimulated excite but little. Not that the muscles exhibit- ing the rigidity are absolutely unamenable to transient spinal reflexes. The extensor- thrust and certain crossed reflexes are witness to the contrary. And they are not absolutely unamen- able to cortical excitation. The extension of the elbow obtain- able from the cortex refutes that. But these instances do not efface the broad fact that a wide system of musculature, includ- ing the extensors of the hip, knee, shoulder, and elbow, and the elevators of the tail, neck, and jaw, is inhibited by the

overwhelming majority of local spinal reflexes and of reactions from the motor cortex, but on the contrary is excited in a set of reflex reactions which employ the local deep afferents (pro- prioceptive) and some cranial mechanism seated between cere- brum and bulb. The cerebellum at once rises to mind. But ll found ablation of the cerebellum did not abolish the rigidity. It is significant that a vertical posture favors the appearance and development of the rigidity. The muscles it predominantly affects are those which in that attitude antagonize gravity. In standing, walking, running, the limbs would sink under the body's weight but for contraction of the extensors of hip, knee, ankle, shoulder, elbow; the head would hang but for the re- tractors of the neck ; the tail and jaw would drop but for their elevator muscles. These muscles counteract a force (gravity) that continually threatens to upset the natural posture. The force acts continuously and the muscles exhibit continued action, ^ tonus. We seem to have here a field of muscles combined as ; a physiological entity. A characteristic reaction yielded by ; muscles of this field is the ** jerk," the " tendon phenomenon," | itself a sign of highly maintained reflex tonus. J

Two separable systems of motor innervation appear thus I controlling two sets of musculature: one system exhibits those transient phases of heightened reaction which constitute reflex movements; the other maintains that steady tonic re- ; sponse which supplies the muscular tension necessary to j attitude. Starting from the tonic innervation as initial state \ the first step in movement tends to be flexion and involves j under ** reciprocal innervation " an inhibition of the extensor ] excitation then in process. This will be involved whether the \ excitation be via local reflex or via the motor cortex. Hence : the very muscles that to the observer are most obviously under \ excitation by the tonic system are those most obviously in- ; hibited by the phasic reflex system. And the tonic system '■■ will, on inhibition of it passing off", contribute toward a return ^ movement to the pre-existing pose, thus having its share in , alternating movements and in compensatory reflexes. These \ two systems, the tonic and the phasic reflex systems, co-operate \

exerting influences complemental to each other upon various units of the musculature. Drugs and other agents that act in a selective way upon nervous processes might be expected in some cases to throw into relief the operation of one or other member of this paired system. Strychnine and tetanus toxin administered to an animal in decerebrate rigidity increase that rigidity. The posture assumed by the limbs, neck, tail, head, etc., in strychnine poisoning and in tetanus resembles closely in many respects the attitude of decerebrate rigidity. There are differences, — for instance, the ankle is often rigidly extended in tetanus whereas it is little affected in decerebrate rigidity ; nevertheless there is much general resemblance.

And just as certain agents display their action more obvi- ously in one member of these paired systems than in the other so processes of disease may be expected to deal with the two systems ^^equally and to reveal more obviously and affect more deeply one of them than the other. Hughlings Jack- son'^'®»^^ with characteristic penetration of thought argued nearly thirty years ago that rigidity ensuing in hemiplegia (hemiplegic contracture) is not owing to the cerebral lesion nor to the lateral sclerosis. He said : " Whilst the primary cere- bral lesion can account for the paralytic element it cannot (nor can the sclerosis of the lateral column) account for the tonic condition of the muscles. My speculation is that the rigidity is owing to unantagonized influence of the cerebellum. Whilst the cerebrum innervates the muscles in the order of their action from the most voluntary movements (limbs) to the most auto- matic (trunk), the cerebellum innervates them in the opposite order. This is equivalent to saying that the cerebellum is the centre for continuous movements and the cerebrum for chang- ing movements. Thus in * walking ' the cerebellum tends to stiffen all the muscles ; the changing movements of walking are the result of ceiebral discharges overcoming in a particular and orderly way the otherwise continuous cerebellar influence. When the influence of the cerebrum is permanently taken off by disease of the cerebrum, as in hemiplegia, from the parts which it most specially governs (arm and leg) the cerebellar

influence is no longer antagonized; there is unimpeded cere- I bellar influx and hence rigidity of the muscles which in health i the cerebrum chiefly innervates. The spinal muscles are those which the cerebrum influences least and the cerebellum most. 'I In health the whole of the muscles of the body are doubly I innervated — innervated both by the cerebrum and cerebel- I lum : there being a co-operation of antagonism between the j two great centres." i

This view of Hughlings Jackson seems supported and i amplified by Luciani and Stefani's work on the cerebellum. ^ Wernicke,^^^^ Mann,^^* and Lewandowski ^^^ also point out that j cerebral paresis selects one group of antagonistic groups of i muscles in the limbs. We may very likely have to seek in the i afferent nerves of muscles — especially of those antagonizing i gravity — and in the nerve of the otic labyrinth — the " tonus- ^ labyrinth" of Ewald — the sources of the influence to which* HughHngs Jackson refers as "cerebellar," but that does not i radically aflect in its main feature the scheme he draws of a" changeful ** clonic " (I would prefer to say " phasic") innervations and a relatively unchanging tonic innervation as two systems in I co-operative antagonism. Although we must also admit that ^ the cortical innervation, pre-eminently phasic though it be, also ^ is to some extent tonic ; Lewandowski's ^^ study of hemiplegic i contracture seems to make this certain.

And here arises a question concerning the neural tonus ] of the skeletal musculature. Since Brondgeest's experiment t neural tonus has been demonstrated to exist in various muscles i and to be of reflex origin. It has however remained a question^ whether a// skeletal muscles habitually exhibit a reflex tonus | or only some of them. Various experiments (Heidenhain, i Wundt) failed to discover reflex tonus in the muscles examined i by them. If the reciprocal innervation of antagonistic muscles ] which obtains in so many reflexes obtains also in the tonic ^ reflexes maintaining neural tonus in muscles, it is obvious thati when one muscle of an antagonistic pair exhibits reflex tonus I its antagonist will not exhibit reflex tonus, but on the contrary | a slight degree of reflex inhibition. We have as yet no clear |

evidence on this. The feeble steady excitation which is the sign of reflex tonus is often difficult to demonstrate. Feeble steady inhibition would be even less easy to detect. But the selective distribution of the jerk-phenomena, under the ordinary conditions employed for their elicitation, to single members of antagonistic couples e. g.^ glutaeiis^ vasto-crureus , masseter, and their absence, under those conditions, from the opposite members of the couples, is suggestive that, under the condition taken, reflex tonus may be confined to one member of each antagonistic pair, namely to that member which is then in reflex tonic operation, e, g. counteracting gravity for the preservation of an habitual pose of the animal.

I have laid some stress on the broad resemblance between the movements elicitable from the motor cortex and those of local spinal reflexes. There are broad differences as well. Spinal reflex movements suggest fairly obviously protective, procreative, or visceral functions on the one hand, and on the other the main movements of the progression habitual to the animal. They seem to refer to stimulation of noci-ceptive or sexual skin nerves or visceral afferent fibres, as though initiated by these. They carry little unequivocal reference to " touch." The existence of spinal reflexes elicited by pure " touch " — apart from that noxious touch evoking scratching-reflexes or eye-blinking — appears to me not established in respect to the normal spinal cord. Similarly in the cat and dog after decere- bration no purely auditory stimulus in my experience excites a reflex,* nor do visual, though the optic tracts and their mid- brain connections have been spared in the decerebration. On the other hand various movements elicitable from the motor cortex carry the significance of possible responses to tactual, auditory, or visual stimuli ; for instance, the closure of the hand, the pricking of the ear, the opening of the eyes, and turning of the head in the direction of the gaze.

Combination of cortical reaction with spinal reflex seems patent in certain reactions of the dog. Thus, the normal dog * I have only seen it do so when the decerebrate animal has been under large doses of atropin. can be seen to, as it were, release, direct, and cut short a scratching reflex (v. s. p. 289). Darwin^ draws attention to a phase of canine behavior in regard to defaecation. ** Dogs after voiding their excrement often make with all four feet a few scratches backward, even on a bare stone pavement, as if for the purpose of covering up their excrement with earth, in nearly the same manner as do cats." In the spinal dog defae- cation is similarly followed by a number of vigorous backward kicks with the hind limbs. The fore limbs I have not been able to observe because the spinal transection has not lain far enough headward to Hberate those limbs for free reflex action. But this movement in the hind limb follows as a reflex in the spinal dog practically invariably in immediate sequence to reflex evacua- tion of the faeces. In the normal dog it is, as Darwin remarked, not invariable ; and it is often not in immediate sequence to the evacuation. The reflex evidently shows modification by cerebral direction and control.

Finally, it seems to me that the number of reflex actions which are " neutral " to each other, in the sense expressed in Lecture II, is less with the cerebral cortex present than without it. This amounts to expressing concretely an inference that the cerebral cortex augments the motor solidarity of the creature. Since there is more solidarity as well as more diversity in those movements of an animal which are directed to its outer environ- ment than to its inner — meaning by this latter the fraction of environment embraced within its own pulmono-digestive cavity — the representation of visceral movement in the cortex will be relatively slight and chiefly concern parts where alimentary canal opens on outer surface.

The reactions of receptor-organs which respond to stimuli from a distance tend especially to have large cortical representa- tion. These receptors tend more than others to control the skeletal musculature of the creature as a whole. The contribu- tion made by the cerebral hemispheres to the solidarity of the motor creature is largely traceable to their bringing to bear on other reflexes the unifying influence of the reactions of the " distance-receptors y This statement may in its baldness appear

doctrinaire ; of that character I hope to relieve it somewhat in the next following Lecture. As to the meaning of this whole class of movements elicitable from the so-called '* motor " cortex, whether they represent a step toward psychical integration or on the other hand express the motor result of psychical integration, or are participant in both, is a question of the highest interest, but one which does not seem as yet to admit of satisfactory answer. In regard to the relatively restricted problem in view in these lectures, namely, the simpler elements of the nervous integration of animal reaction, the motor reactions elicitable from the so- called " motor " cortex furnish evidence confirmatory of points mentioned before in regard to lower reflex action. This is in- teresting, since they must be admitted to be movements of higher order than any of those others. Nevertheless they are to my thinking merely fractional movements ; movements which rep- resent but parts of the nervous discharge which emanates from the brain under the normal working of its unmutilated whole. The results before you must appear a meagre contribution toward the greater problems of the working of the brain ; their very poverty may help to emphasize the necessity for resorting to new methods of experimental inquiry in order to advance in this field. New methods of promise seem to me those lately followed by Franz, Thorndyke, Yerkes, and others ; for instance, the influence of experimental lesions of the cortex on skilled actions recently and individually, /. e, experientially, acquired. Despite a protest ably voiced by v. Uexkiill, comparative psychology seems not only a possible experimental science but an existent one. By combining methods of comparative psychology {e. g. the labyrinth test) with the methods of experimental physiology, investigation may be expected ere long to furnish new data of importance toward the knowledge of movement as an outcome of the working of the brain.

Argument: The primitive reflex-arc. The diffuse nervous system and the gray-centred nervous system ; the central nervous system a part of the latter. Nervous integration of the segment. The three re- ceptive fields. Richness of the extero-ceptive field. Special refine- ments of the receptor-organs of the "leading" segments. The refined receptors of the leading segments are "distance-receptors." " Distance-receptors ; " the projicience of sensations. Extensive internuncial paths belonging to "distance-receptors." "Distance- receptors " initiate precurrent reactions. Consummatory reactions ; strong affective tone of the sensations adjunct to them. Receptive range and locomotion. The " head " as physiologically conceived. Proprio-ceptive arcs excited secondarily to other arcs. Close func- tional connection between the centripetal impulses from muscles and from the labyrinth. Tonic reflexes (of posture, etc.) and compen- satory reflexes are characteristic reactions of this combined system. Nervous integration of the segmental series. Restriction of seg- mental distribution a factor in integration. The cerebellum is the main ganglion of the proprio-ceptive system. The cerebrum is the ganglion of the "distance-receptors."

We may now attempt to gather from the various notions, how- ever fragmentary, that have occupied us, some general con- ception of the neural architecture of an animal as a whole; though of course only in its motor aspect, for its truly sensorial aspects we have hardly had before us. The problem is too difficult for me to expect much success. Yet it will repay us if from the attempt we glean something at least of one cardinal feature of the scheme, namely, the dominance attained by one limited set of neural segments, the brain, over all the rest.

We must allow ourselves at certain points some repetition of considerations already urged, in order to draw from them now in new juxtaposition some further significance. The primitive reflex-arc. — If we seek for a reflex-arc of sim- plest construction it is true we find in some unicellular organisms, e.g. Vorticella, a mechanism which resembles a nervous arc and is quite simple. This mechanism, composed from a single cell, shows differentiation into three parts respectively, — receptive^ conductive, and effective. In Vorticella the receptive element is the ciliated peristome ; a stimulus reaching these cilia at the free end of the cell excites contraction of the myoid filament at the fixed end of the cell. Similarly with the individual cells of Poteriodendron (Verworn). In multicellular organisms of low organization like mechanisms occur. In Actinia there are ectoderm cells which have externally a receptive hairlet and internally a contractile fibre, and this latter contracts when the receptive hairlet is stimulated.

In view of such cases it might have seemed likely that in more highly developed organisms examples would have been forth- coming in which the differentiation of the parts of a single cell would have advanced further still and produced something yet more akin to a simple reflex-arc such as is considered typical of the true nervous system itself. That expectation is not realized, What we find as the simplest arc in the organisms which possess a true nervous system is that the conductor mediating between receptor and effector is itself a separate cell intercalated between a receptive cell and an effector cell. At each end this separate conductive cell breaks up into branches. The branching at the receptive end places it in communication not with one but with several receptor cells. This must allow stimuli at a number of receptive points to combine by summation to a conjoint effect. By this means the threshold of reaction will be lowered and the organism in that respect become more sensitively reactive to the environment. At the deep, i. e. effector, end the branching of the conductive stem places it in touch not with one effective cell but with many. Thus, again, there must result lowering of the threshold — of what we may term the effective threshold. The contraction of a single muscle-fibre in a muscle is practi- cally ineffective where the resistance and mass of the muscle and its load are great as compared with the power of a single muscle- fibre. But by its branching the motor neurone obtains hold of many muscle-fibres. This must tend to lower the effective

threshold of reaction, and thus again the organism is rendered more delicately responsive to stimulation by its environment. But — and it is a striking fact — we do not know of any reflex- arc in which in fact the nervous conductor connecting receptor to effector is formed from end to end of one single neurone. The length of the conductor seems always to include at least two neurones in succession. A moment's reflection reminds us that such arrangements as Vorticella, Poteriodendron, and the neuro- muscular cells of Hydra and Actinia do not exhibit the germ of a feature that we have already considered fundamental in the construction of the reflex nervous system. The cases cited do not exhibit even in germ the co-ordinative mechanism which is attained by the principle of the common path. Such cases con- fine each effector to the use of one receptor only, and confine each receptor to the use of one effector only. But we saw that a great principle in the plan of the nervous system is that an effector shall be at the behest of many receptors, and that one receptor shall be able to employ many effectors. We saw further in respect to this that there are two conditions which the ner- vous system satisfies. One is that the effector is at the behest of various receptors which can use it simultaneously and use it harmoniously all in more or less the same way. Thus an advan- tage accrues in that their reactions sum, even though the re- ceptors may be of different modality; and by summation the threshold is lowered and the organism more sensitized to the environment. This arrangement cannot be obtained by the uni- cellular mechanisms instanced above. It can only be obtained by the formation of a common path, and the formation of a common path can only be rendered possible by having a con- ductor of pluricellular length.

And there is another condition which the nervous system satisfies The unicellular reflex-arc — if reflex-arc it can be called — not only admits no opportu- nity for pluricellular summation but also none for the second function of the jointed reflex-arc of pluricellular length, namely " interference'^ In animals of complex organization the activity of one effector organ may interfere with the function of another, e, g.y in the case of muscles which when contracting pull in

opposite directions at the same lever. We have seen how this wasteful confusion is avoided by one receptor having power not only to throw a particular effector into action but also to throw the opposed effector out of action. We saw that this action it exercises not peripherally but within the nervous system, at the entrance to a common path. The unicellular reflex-arc allows no common path. It lacks, therefore, the mechanism which renders possible the two great co-ordinative processes of pluri- receptive summation and of interference. Without these the nervous system is shorn of its chief powers to integrate a set of organs or an organism.

It is therefore a significant thing that in the nervous system there is not only no instance of the reflex triune — receptor, conductor, and effector — being formed of one cell only, but also no indubitable instance where the middle link, the con- ductor, is even itself formed of one cell (one neurone) only. In other words, we know of no instance in the nervous system of a reflex-arc so constructed as not to include a junction between one neurone and another neurone. And the rule is apparently always that at such junctions not only does one neurone meet another, but several neurones converge upon another and make of the latter a common path.

The diffuse nervous system, the gray-centred nervous system, the central nervous system a part of the latter. The term " nerve- centre " is sometimes abused, yet seems in several ways apt. A keynote regarding that part of the nervous system which is termed " the central " seems that it is wholly pieced together into one system. The nervous system in its simplest forms^is\ diffuse — a number of scattered mechanisms performing merely local operations with much autonomy save that they have com- munication with their immediate neighbors across near bound- aries. The co-ordination effected by the diffuse nervous system is not adapted to compass the quickly combined action of dis- tant parts. It is slow, and it throws en route the effectors of intermediate regions into action. It is ill suited, therefore, to produce the integration of a large and complex individual as a whole, or even to integrate large differentiated portions of an

individual. Yet the co-ordination it brings about in its own local field may be strikingly effective. A co-adjustment though simple and restricted may be not less perfect than one involving wide and complex neural mechanism. ] The co-ordination of a peristaltic movement of the bowel is, as shown by Bayliss and Starling, even when managed exclusively by the local diffuse nervous system, capable of the perfect taxis of two muscular coats arranged antagonistically in the viscus. It directs a relaxa- tion of the one co-ordinately with a contraction of the other ; it exhibits a primitive but none the less perfect form of " recipro- cal innervation."

This diffuse system seems the only one in such an organism as Medusa. But in higher animals a system of longer direct connections is developed. And this latter is " synaptic," that is, possesses the adjustable junctions which belong characteristically to " gray matter." This synaptic system co-existing with the diffuse in various places dominates the latter. Thus it controls and overseers the actions of the local nervous system of the vis- cera, and heart, and blood-vessels, which even in the highest animal forms remain diffuse.