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1 ON THE EFFECT OF ARTIFICIAL STIMULATION OF THE RED NUCLEUS IN THE ANTHROPOID APE. BY T. GRAHA.M BROWN. (From the Laboratory of Experimental Physiology of the University of Manchester.) THE author has previously shown that stimulation of certain points in the cross-section of the mid-brain at the level of the anterior colliculi in monkeys yields characteristic reactions'. The small areas from which these reactions may be obtained lie on eitlher side of the mid-line some millimetres ventral to the neuraxial canal (aqueduct of Sylvius). It appeared that the area might correspond with the anatornical position of the red nucleus (or perhaps with that of the posterior longitudinal bundle). The reactions obtained proved to be evoked with regularity in different individual monkeys and to present certain definite characteristics. Thus stimulation applied to this area of the cross-section of the mid-brain on one side evoked a state of flexion in the arm of the same side and a state of extension in the arm of the opposite side. On cessation of stimulation these reactions are continued as maintained postures. The movements of the armns are accompanied by movements of other parts of the body. The tail seems to bend to the same side; the lower limb of the same side extends while that of the opposite side flexes; the head is rotated in such a manner that the face is turned away from the side stimulated. Such at any rate seem to be the usual postures assumed. Last summer an opportunity presented itself for the examnination of these reactions in the decerebrate chimpanzee. The animal was a large one, but it was thin and in a bad and dirty condition. It must be noticed, however, that monkeys in bad condition often give the best experimental results, and in the case of this ape certainly the results obtained for various observations extending over many hours were good. 1 Proc. Roy. Soc., B, LZXXVII. p
2 186 T. GRAHAM BROWN. After amputation of the left hand at the wrist and motor paralysis of all the muscles acting upon the left shoulder and elbow, with the exception of supinator longus and the humeral parts of triceps (the scapular head of which was cut across), these two muscles were arranged separately for the recording of their movements on the double myograpb. Their origins were firmly fixed by means of strong steel rods drilled into the head of the humerus and through its lower end. Stimulation of the areas investigated was caxried out in the uni-polar method-the large indifferent electrode being applied to the sole of the right foot. Decerebration, which was performed after the animal had been under a chemical narcotic for about 6 hours and 50 minutes, was first done at a high level for another purpose. A second decerebrating lesion was made 35 minutes later in such a manner that the neuraxis was cut across about 3 mm. above the anterior colliculi. The plane of section was not quite at right angles to the longitudinal axis of the nervous system. The effects of stimulation of the points in the crosssection of the neuraxis were examined about 1 hours after the cessation of the chemical narcosis. The animal was of course kept completely unconscious throughout the whole experiment and until it died at the termination of it. When the effects of stimulation of points near the red nuclei on the cross-section of the mid-brain were tested it was found that the contralateral reaction (that evoked in the left arm muscles on stimulation applied to the red nucleus point on the right side of the c-ross-section) was one of flexion, and that the flexion was maintained after cessation of stimulation (Fig. 1). Stimulation of the corresponding ipsilateral point gave a much larger flexion reaction, and this also was maintained. A second stimulation which was applied to the contralateral point during this after-discharge of the ipsilateral reaction had no effect upon it. In this case the ipsilateral flexion reaction is "normal" but the contralateral flexion is not the usual reaction. In the monkey contralateral extension is the rule. It is possible that the uni-polar electrode was applied too near to the mid-line and that the strength of stimulus used was too great-so that a " spread " effect to the ipsilateral red nucleus occurred and overbore the true contralateral extension reaction. It is also possible that a true contralateral flexion reaction sometimes occurs. In the monkey bilateral extension of the arms may sometimes be obtained on stimulation of a point on the surface of the cross-section of the mid-brain external to the area of the red nucleus.
3 RED NUCLEUS REACTIONS. 187 Sulpinatol 1II 0 1 H4. 1Tr-iceps. Sign,al. Secoinds. Fig. 1. Decerebrate chimpanzee, Troglodytes niger. A record obtained about 55 minutes after decerebration. In this record the stimulus is first applied (K-L, A) to the contralateral red nucleus on the cross-section of the mid-brain at (or a little in front of) the anterior colliculi. The reaction obtained is one of contralateral flexion-as is shown by the contraction of a flexor muscle (upper myograph line). On cessation of stimulation (at L-1, 1') there is seen to remain a state of maintained flexor contraction. The stimulus is then applied to the ipsilateral (left) red nucleus- G-H-and a similar flexion reaction, but of greater extent, is obtained. This is followed by a well-marked flexor after-discharge during which a second stimulation of the contralateral red nucleus-k-l, B-has no further effect. In this and in the succeeding figures the upper myograph line registers the movements of a flexor muscle in the left arm-supinator longus. The lower myograph line similarly registers the movements of an extensor-humeral parts of triceps. The rise of the curve denotes contraction and the fall relaxation of the muscle. The signal line gives the relations of commencement and termination of stimulation. These points are marked with the letters K and L for stimulation of the contralateral (right) red nucleus, and G and H for stimulation of the ipsilateral (left)
4 188 T. GRAHAM BROWN. red nucleus. Ordinates corresponding to these marks on the signal line have been drawn upon the two myograph lines after the record had been taken and while the drum was stationary. These ordinates are lettered k', I' and 9', W for the flexor myograph line and k, I and g, h for the extensor myograph. Where, in a record, the stimulus is applied more than once to the same point the successive stimulations are marked A and B or I and IL The strength of stimulus used is marked below the signal line-for instance, " 3000 K.U. " in the present figure. This figure refers to the number of Berne units in the induction coil used in these experiments. Time is marked in seconds on the lowest line of the records; and a millimetre scale has been drawn on each record before it was varnished-so that the scale is reduced in reproduction in the same proportion as the record itself The ordinates drawn at the beginning and end of each record for the two myograph lines are accurate and synehronise with the marks at the beginning and end of the signal line. The ordinates drawn in the record to mark the time relations of the commencement and termination of stimulation are not necessarily correct, but may be corrected by reference to the others. They are drawn after the end of the experiment and, as the long paper may slip upon the drums of the kymograph, -small inaccuracies may occur-although steps are taken to correct these small errors as far as is possible. Five minutes after this first test of the red nucleus points they were again stimulated (Fig. 2). The contralateral stimulus now gave an exceedingly sharp relaxation of the maintained flexor contraction which was in being at the time of its application, and this relaxation was accompanied by a marked extensor contraction. On cessation of stiinulation there was a sharp relaxation of the extensor contraction and a contraction of the flexor-in other words there was a flexion "rebound" phenomenon. Six seconds later the ipsilateral red nucleus was stimulated and the reaction evoked consisted in a flexor contraction which persisted as flexor after-discharge on cessation of stimulation. About five seconds later the contralateral red nucleus was again stimulated and there occurred as before a sharp relaxation of the maintained flexor contraction and a contraction of the extensor. On cessation of stimulation this contraction did not at once pass into a sharp relaxation as was the case in the response to the first contralateral stimulus, but slowly fell. This slow fall of extensor contraction was accompanied, about 2'5" after the cessation of stimulation, by a slow rise of flexor contraction. A final stimulus applied to the ipsilateral red nucleus now evoked extensor contraction (Fig. 2). Three minutes later these observations were repeated with a less great strength of stimulus (Fig. 3). The contralateral reaction now was still one of extension-extensor contraction and flexor relaxation-but on cessation of stimulation the extensor after-discharge was much better sustained than before. The ipsilateral reaction consisted in flexqr contraction and extensor relaxation, and it was-followed by flexor after-discharge. In
5 RED NUCLEUS REACTIONS. 189 _ J *_- _:: :r_.j C. C' ~r_
6 190 T. GRA HAM BRO WN. fact the two reactions at this point in the experiment may be regarded as typical. A second stimulation of the contralateral red nucleus was accompanied and followed by the same effects as before, but the initial extensor contraction was a much sharper movement (Fig. 3). Suapinator Sleconds. Fig. 3. Decerebrate chimpanzee, Troglodytes niger. A record from the same experiment as the two preceding figures and obtained three minutes after that reproduced in Fig. 2. The strength of stimulus here used (2000 K.u.) is less than before. In this record the stimulus is first applied to the contralateral red nucleus (K-L, I). The reaction is one of extension and is better marked than before. It is succeeded by an after-discharge of maintained extension which for about 4" is retained at a high level and then gradually falls. The ipsilateral red nucleus is then stimulated (G-H) and gives a reaction of flexor contraction and extensor relaxation. On cessation of stimulation there is first a rapid fall of flexor contraction but this is soon arrested and there then persists a certain degree of maintained flexor after-discharge. This is relatively and absolutely much less than the flexor afterdischarges in the two preceding figures. Finally the contralateral red nucleus is again stimulated (K-L, II). There again occur extensor contraction and flexor relaxation. The latency of these movements is much shorter than before, and they appear to be sharper. The extent of extensor contraction is, however, less-but it must be noted that the duration of the period of stimulation is here comparatively brief.
7 RED NUCLEUS REACTIONS. 191 S1iiiuiuator Trice1)p.,Sional. MCc. Fig. 4. Decerebrate chimpanzee, Troglodytes niger. A record obtained in the same experiment as the preceding figures and three minutes after Fig. 3. In this figure the contralateral red nucleus is first stimulated (K-L). The reaction, as before, is one of extensor contraction and flexor relaxation. The extensor contraction is greater in extent than before, and in fact the extensor lever came into contact with that of the flexor. The extensor lever was carried off the recording surface but its line ran parallel to that described by the flexor lever (under this interference) from the point at which the extensor myograph line strikes the abscissa of the flexor myograph to the point at which the extensor again records near 9'. On cessation of stimulation (L-1, I') there is a very well-marked maintained extensor after-discharge. The ipsilateral red nucleus is then stimulated (G-H). There is a reaction of flexor contraction and extensor relaxation during the period of stimulation, but it will be observed that on cessation of stimulation (at h, h) there occur a sharp flexor relaxation and a well-marked extensor contraction-extensor "rebound." These four figures therefore demonstrate a series of red nucleus reactions which show variations in the relative values of flexion and extension from reactions in which flexion seems to preponderate to reactions in which extension does-the relative preponderance of one or other of these factors being perhaps most clearly exhibited in the various terminal phenomena seen on cessation of the evoking stimuli.
8 192 T. GRAHAM BROWN. After another three minutes the points were again stimulated (Fig. 4) with the same strength of stimulus as in the immediately preceding observation. The contralateral reaction showed the same features as before but the height of extensor contraction attained was greater than that in the preceding observations and the extensor after-discharge which persisted after cessation of stimulation was much better sustained. In the immediately preceding observation the extensor after-discharge remained at a height of extensor contraction equal to or greater than that during the application of the stimulus for about 4" and then slowly fell until, 5" later, it was about half its initial height. In the present observation the extensor contraction in after-discharge showed no sign of fall for the 5" which intervened before the ipsilateral red nucleus was stimulated. Stimulation of the ipsilateral red nucleus was accompanied by a slow fall of the extensor contraction then in being and a slow rise of flexor contraction. At the point of withdrawal of the stimulus there was a sharp flexor relaxation accompanied by a well-marked extensor contraction-in other words, an extension " rebound " phenomenon (Fig. 4). In a final series of stimulations a point of interest was noticed. Stimulation of a point in the cross-section of the contralateral pyramidal tract was accompanied by flexion of the arm-cessation of stimulation being followed by sharp flexor relaxation as is usual in these pyramidal tract reactions. When such a reaction was evoked against a background formed by the maintained extensor contraction of the after-discharge from the contralateral red nucleus reaction there was no interference with the extensor contraction during the period of the application of the stimulus; but a sharp relaxation of the maintained extensor contraction occurred immediately on withdrawal of the stimulus. This observation is curious in view of the post-stimulatory abolition of the maintained flexor contraction of the ipsilateral red nucleus reaction observed under the same circumstances in the monkeyl. These observations on the effect of stimulation of the red nucleus by the uni-polar method in the chimpanzee seem on the whole to correspond with the observations in the monkey. The usual contralateral reaction appears to consist in a movement of extension (extensor contraction, flexor relaxation) of the arm during the period of stimulation, and of a maintenance of this extension after the cessation of the stimulus. The ipsilateral reaction appears usually to consist of a movement of flexion (flexor contraction, extensor relaxation) of the arm 1 Proc. Roy. Soc., B, LxXXVi. p
9 RED NUCLEUS REACITIONS. 193 during stimulation and of a maintenance of this flexion after the cessation of the stimulus. But variations of these usual occurrences sometimes are seen. Thus in certain circumstances the contralateral reaction may be one of flexion, and then the ipsilateral flexion reaction also occurs and is unusually well marked. Even when the contralateral reaction is one of extension during the period of stimulation there may be no maintenance of this after cessation of the stimulus. There is then a sudden relaxation of the extensor contraction and a well-marked flexor contraction-in other words, no maintained extensor after-discharge but a flexor rebound contraction of maintained form. When this occurs the ipsilateral reaction still exhibits well-marked flexion phenomena. In other cases there may be badly-marked maintained extensor after-discharge on cessation of stimulation in the contralateral reaction, and this may yield place to flexor contraction. In such cases the flexion of ipsilateral reaction is perhaps not so well marked as before but there is still a good after-discharge of flexor contraction. Finally the contralateral reaction may consist in well-marked extension during stimulation and, on withdrawal of the stimulus, an after-discharge of extensor contraction which is extremely well maintained. When this is the case the ipsilateral reaction may not be followed by a flexor maintained after-discharge but actually by a relaxation of flexor contraction and a maintained extensor contraction. Finally in some cases the ipsilateral reaction appears to be one of extension and not the usual flexion phenomenon. In the present experiment all these different variations (with the exception of the last) were observed in the above order. During the course of the experiment the strength of stimulus was once changed, but this change can hardly be regarded as the sole condition of the variation of results. In the different observations approximately the same points on the cross-section of the mid-brain (red nuclei areas) were stimulated. Yet at the beginning of the series of observations flexion phenomena, and at the end of them extension phenomena, preponderated. A physical change concomitantly took place in the preparation of the mid-brain. At the commencement of the series it had been well protected from its surroundings by pads of warm moist cotton-wool. During the series of observations it certainly cooled, although precautions were taken to avoid this cooling as far as was possible. Apart from this, the experiments were made at the end of a long experiment. The animal actually died about half an hour after the last of them.
10 194 T. GRAHAM BROWN. In any case 'the change during this series of observations from reactions which exhibit a preponderance of flexion to reactions which exhibit a preponderance of extension is one of interest. We may grant that the main effect of the stimulation of one red nucleus is a movement of flexion in the arm of the same side and a movement of extension in the opposite arm-these movements, having attained their maximum, tending to be maintained long after cessation of the evocative stimulus. It is possible to explain the variations in the results here obtained in one of two manners. In the first place it is possible that when one red nucleus is stimulated in the uni-polar method the other is also stimulated (but to a less degree) by " spread " of current. This mnust be so physically; the possibility here suggested is that stimulation by "spread" of current is effective physiologically. When stimuli of comparatively weak strength are uised this " spread" is probably not effective; but granting that it is so effective the reaction in a single arm might be a compound one conditioned by the effects upon its spinal centres of the activities of the two red nuclei. That is, it might be a compromise between the flexion conditioned by the activity of the red nucleus of the same side and the extension conditioned by that of the opposite red nucleus. Thus with varying values of stimulation (conditioned for instance by a change in the state of the preparation) varying values of contralateral extension and ipsilateral flexion might compound to give reactions in which extension and flexion exhibited differing preponderancies. The other possibility is that the activation of a single red nucleus is a mixed one-that while the chief action of a red nucleus on the arm of the same side is one of flexion it also has an effect (although a weaker one) of extension, and that while its chief contralateral effect is one of extension it also has an effect of flexion. Then the different values of stimulation applied to one red nucleus might evoke reactions in which the extension and flexion factors had different intensities. The present experiment offers no data for the positive conclusion as to which of these two possibilities is the true explanation of the phenomena obtained. The question might be settled if reactions which vary in the manner of the reactions described in this paper were obtained by the stimulation of one red nucleus after the removal of the other lateral half of the mid-brain to eliminate the possibility of "spread " of stimulating current to the other red nucleus.
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