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1 547 J. Physiol. (I955) I29, SPLENIC FUNCTION IN RELATION TO BLOOD PRESSURE CHANGES EVOKED BY STIMULATION OF THE CEREBRAL CORTEX BY P. J. KLOPPER Department of Physiology, University of Amsterdam (Received 11 February 1955) Many authors have demonstrated that the cerebral cortex influences arterial pressure. These experiments were performed on several species of animals and also on man. The most recent publications are those of Lund (1945), Livingston, Fulton, Delgado, Sachs, Brendler & Davis (1948), Kaada (1951) and Wall & Davis (1951). The cortical areas exercising this action include the motor area and the prefrontal area (Lund, 1945; Morin, Zwirn & Corriol, 1952, Morin & Zwirn, 1953; Morin, Corriol & Zwirn, 1953; Eliasson, Lindgren & Uvnais, 1952); the orbital gyrus (Sachs, Brendler & Fulton, 1949; Hess, Akert & McDonald, 1952); the limbic area (Smith, 1945; Ward, 1948; Kaada, 1951) and some parts of the temporal lobe (Wall & Davis, 1951; Hoffman & Rasmussen, 1953). Changes of arterial pressure have also been caused by stimulation of the sensorimotor cortex and the orbital gyrus (Klopper, 1954). It further appears possible to cause both rises and falls of blood pressure by stimulating the tip of the temporal lobe in cats (gyrus ectosylvius post. and gyrus sylvius post.). This had previously been demonstrated in Primates and also in man by Kaada (1951), Wall & Davis (1951) and Chapman, Livingston & Poppen (1950). The aim of the experiments described here was to ascertain whether the spleen plays any role in the changes of arterial pressure evoked by stimulation of the cerebral cortex. The literature contains only a few reports on the influence of the cerebral cortex on splenic function. Bochefontaine (1875) reported that splenic contractions were evoked after stimulation of the sigmoid gyri in dogs. Barcroft & Stephens (1927) found that the emotional state of the animal influences the degree of contraction of the spleen. Bykow (1947) showed on dogs that the cerebral cortex has an influence on the spleen. He found that conditioned reflexes on the spleen could be formed.
2 548 P. J. KLOPPER The role of splenic function in the establishment of arterial pressure changes is also little known. Barcroft, Harris, Orahovats & Weiss (1925) showed that the spleen has the capacity to release an amount of blood into the circulation if required. In the cat this quantity amounts to % of the total volume of circulating blood (Hamilton, 1950). Granaat (1952) caused a contraction of the spleen by stimulating the efferent nerves of the plexus lienalis; this was accompanied by an arterial pressure rise of mm Hg. Granaat (1952, 1953) showed that these rises are caused by hypertensive substances, including noradrenaline, produced by the spleen. He is of opinion that the arterial pressure rise following contraction of the spleen can be ascribed only in part to the increase of circulating blood volume, occurring with splenic contraction. In the experiments described here the spleen was excluded from the circulation after it had been demonstrated that the cerebral cortex influences the arterial pressure. The question studied was whether the spleen, either by releasing an amount of blood into the circulation or by secretory action, plays a role in the production of arterial pressure changes evoked by stimulation of the cerebral cortex. METHODS The experiments were performed on thirty cats with a mean weight of 3 kg. Ether, chloralose with urethane, pentobarbital and thiopentone were used for anaesthesia, sometimes in combination. After basal anaesthetization with pentobarbital or chloralose-urethane solution the anaesthesia was continued with ether or thiopentone. Some further experiments were performed using ether anaesthesia with D-tubocurarine. The arterial pressure was recorded with a mercury manometer, the respiration with a tambour system. After opening the cranium and the dura, the cerebral cortex was stimulated with a square-wave stimulator. The stimulation was performed with two thin enamelled wires fixed in a small holder. The points of these wires were 1-2 mm apart. The spleen was excluded from the circulation by a Schoemaker clamp placed over the splenic hilus or by separate double ligation of the vessels, and thereupon extirpated. Three experiments were made after extirpating the spleen a considerable time previously (from a few days to several weeks). RESULTS Stimulation of the dorsal surface of the frontal lobe The stimulated area was situated on the anterior and posterior sigmoid gyri. The frequency of the stimulus with which optimal results were obtained, both for the rise and for the fall of arterial pressure, was 15-20/sec with an impulse duration of msec. The intensity varied from 0 05 to 0'6 ma. Examples of the effects of stimulating the same cortical area before and after extirpation of the spleen are represented in Figs. 1 and 2. In Fig. 1 a pressure rise is shown. Stimulation of the same cortical area after removal of the spleen produces a pressure fall (Fig. 2). Effects of this kind were repeatedly obtained.
3 CEREBRAL CORTEX AND SPLEEN 549 It was also observed that the pressure fall caused by stimulating the dorsal area of the frontal lobe after extirpation of the spleen was several times larger than that evoked before this procedure. The stimulus intensity was the same in both experiments. Fig. 1. Stimulation of the dorsal frontal cortex near the sulcus coronalis. Stimulus frequency: 16/sec. Impulse duration: 15 msec. Intensity: 06 ma. Upper line: time marker 2 sec. Middle line: signal line. Fig. 2. Stimulation of the same area after extirpation of the spleen. Stimulus: as in Fig. 1. It appears from these experiments that the spleen plays an important role in the rise of arterial pressure on electrical stimulation of the frontal area. It can be further concluded that the spleen has a function in the stabilization of arterial pressure.
4 550 P. J. KLOPPER Stimulation of the orbital gyrus Stimulation of the orbital gyri was followed by both rises and falls of blood pressure. The pressure rises evoked by electrical stimulation were not influenced by excluding the spleen from the circulation. It may be concluded from these experiments that the spleen has no relation to the rise of blood pressure evoked by stimulation of the orbital gyrus. Stimulation of the temporal lobe The temporal cortical area that was found to influence the arterial pressure was situated on the posterior sylvian and posterior ectosylvian gyri. In a number of animals the spleen was extirpated after it had been ascertained that stimulation of the temporal cortex gave rise to distinct changes in arterial pressure. The rise of blood pressure evoked by stimulating the temporal cortex did not occur after the spleen had been cut out of the circulation. An example is given in Figs. 3 and 4. In these figures the blood-pressure curves evoked by stimulation of an area situated dorsally to the sulcus sylvius are represented. A stimulus with a frequency of 15/sec, an impulse duration of 10 msec and an intensity of 041 ma evokes a well-marked response of the blood pressure. This is characterized by both rise and fall and by the long duration of the effect. The period of stimulation is 25 sec while the effect continues for about 3 min. The respiration is not altered with the exception of one movement provoked by movement of the animal. Fig. 4.shows the result of stimulating the same area after extirpation of the spleen. This time there is no rise of blood pressure. These experiments show that after extirpation of the spleen no blood-pressure rise could be evoked by stimulating the temporal cortex. To verify the results obtained in the acute experiments the following further experiments were carried out. A considerable time before the experiment (from several days to several weeks) the spleen was extirpated in a number of animals. The experiments were made after the animals had completely recovered. The cerebral cortex was stimulated as described above. Both the frontal and the temporal cortex were stimulated. In no case was any rise of arterial pressure obtained. The experiments on splenectomized animals thus confirm the results obtained in acute experiments. DISCUSSION The experiments described show that extirpation of the spleen influences the blood-pressure changes evoked by stimulating certain areas of the cerebral cortex, viz. the temporal lobe and the dorsal surface of the frontal lobe. On the other hand, the rise of arterial blood pressure produced by stimulation of the orbital gyrus remained unchanged after extirpation of the spleen.
5 CEREBRAL CORTEX AND SPLEEN 551 Fig. 3. Stimulation of the temporal cortex near the sulcus sylvius post. Stimulus: 15/sec; 10 msec; 0 1 ma. Above blood pressure: record of respiration. Fig. 4. Stimulation of the same area as in Fig. 3 after extirpation of the spleen. Stimulus: as in Fig. 3.
6 552 P. J. KLOPPER In the cat no direct relationship between the temporal cortex and the sensorimotor cortex has been demonstrated. In Primates, however, Wall & Davis (1951) found that the temporal cortex and sensorimotor cortex have in common the fact that the changes of blood pressure evoked by stimulating them are not influenced by destruction of the hypothalamus. It can be concluded that splenic function is influenced by the cerebral cortex. This is in accordance with the results of Bykow (1947) who was able to form conditioned reflexes on the spleen. It appears that the temporal and frontal cortex acts at least in part via the spleen. It is likely that the pressure rise evoked by stimulating these cortical areas is to be ascribed partly to splenic action. This organ can, as previously mentioned, influence the blood-pressure level either by releasing an amount of blood into the circulation or by secreting hypertensive substances. From the experiments concerning the influence of the orbital gyrus on arterial pressure it appears that extirpation of the spleen does not influence the rise evoked by stimulation of this area. This may be explained by the observations of several authors who have studied the conduction of impulses from the orbital gyrus to lower centres of the central nervous system which influence arterial pressure. In apes, dogs and cats Sachs & Brendler (1948) showed that the impulses from the orbital gyri influencing arterial pressure go by way of the hypothalamus to the lower vasomotor centres. Wall & Davis (1951) confirmed this in apes and showed also that the impulses influencing arterial pressure from sensorimotor and temporal cortex do not pass through the hypothalamus. SUMMARY 1. Rise and fall of arterial pressure in the cat was evoked by the stimulation of two specified areas on the ventral and dorsal surfaces of the cortex of the frontal lobe. Fluctuations of arterial pressure were also caused by stimulation of a specified area on the temporal lobe. 2. The spleen appeared to have considerable influence on those changes of arterial pressure which took place after stimulation of the dorsal area of the frontal cortex and the area on the temporal cortex. 3. The spleen undoubtedly plays an important role in the rise of arterial pressure following electrical stimulation of the frontal and temporal areas. After the elimination of splenic influence, stimulation of the dorsal part of the frontal lobe and of the temporal cortex evoked only a fall of arterial pressure. 4. The rise of arterial pressure evoked by stimulation of the orbital gyrus appeared to be unchanged after the elimination of the splenic influence.
7 CEREBRAL CORTEX AND SPLEEN 553 REFERENCES BARCROFT, J., HARRIS, H. A., ORAHOVATS, D. & WEISS, R. (1925). A contribution to the physiology of the spleen. J. Physiol. 60, BARCROFT, J. & STEPHENS, J. G. (1927). Observations upon the size of the spleen. J. Physiol. 64, BOCHEFONTAINE, L. T. (1875). Contribution a l'etude des effets produits par l'excitation electrique du cerveau. C.R. Soc. Biol., Paris, 27, BYvow, K. M. (1947). Cerebral Cortex and the Visceral Organs (Russian), 2nd ed. Moscow. CHAPMAN, W. P., LIVINGSTON, K. E. & POPPEN, J. L. (1950). Effect upon blood pressure of electrical stimulation of tips of temporal lobes in man. J. Neurophysiol. 13, ELIASSON, S., LINDGREN, P. & UVNAS, B. (1952). Representation in the hypothalamus and the motor cortex in the dog of the sympathetic vasodilator outflow to the skeletal muscles. Acta physiol. scand. 27, GRANAAT, D. (1952). De milt in de regulatie van de arteriele bloeddruk. Thesis, Amsterdam. GRANAAT, D. (1953). The spleen in the regulation of the arterial blood pressure. J. Physiol. 122, HAMILTON, W. F. (1950). Circulation through special regions. Chapter 38, in FULTON, J. F. A Textbook of Physiology, 16th ed. Philadelphia. HESS, W. R., AKERT, K. & MCDONALD, D. A. (1952). Functions of the orbital gyri of cats. Brain, 75, HOFFMAN, B. L. & RASMUSSEN, T. (1953). Stimulation studies of insular cortex of Macaca mulatta. J. Neurophysiol. 16, KAADA, B. R. (1951). Somato-motor, autonomic and electro-corticographic responses to electrical stimulation of 'rhinencephalic' and other structures in Primates, cat and dog. Acta physiol. scand. 24, suppl. 83, KLOPPER, P. J. (1954). De invloed van de schors van de grote hersenen op enige autonoom geinnerveerde organen. Thesis, Amsterdam. LIVINGSTON, R. B., FULTON, J. F., DELGADO, J. M. R., SACHS, E., Jr, BRENDLER, S. J. & DAVIS, G. D. (1948). Stimulation and regional ablation of orbital surface of frontal lobe. Res. Publ. Ass. nerv. ment. Di8. 27, LUND, A. (1945). The function of the cortical vasomotor centres elucidated through experimental studies on animals. Acta psychiat., Kbh., 20, MORIN, G., CORRIOL, J. & ZWIRN, P. (1953). Signification de l'hypertension art6rielle provoqu6e par la stimulation 6lectrique du gyrus sigmolde. J. Physiol., Paris, 45, MORIN, G. & ZWIN, P. (1953). La voie pyramidale intervient-elle dans les hypotensions art6rielles obtenues par stimulation du cortex moteur chez le chien narcose? J. Physiol., Paris, 45, MORIN, G., ZwIRN, P. & CORRIOL, J. (1952). Influence de la narcose sur les variations de pression arterielle provoquees par stimulation du gyrus sigmolde. C.R. Soc. Biol., Paris, 146, SACHS, E., Jr, & BRENDLER, S. J. (1948). Some effects of stimulation of the orbital surface of the frontal lobe in the dog and monkey. Fed. Proc. 7, 107. SACHS, E., Jr, BRENDLER, S. J. & FULTON, J. F. (1949). The orbital gyri. Brain, 72, SMITH, W. K. (1945). The functional significance of the rostral cingular cortex as revealed by its responses to electrical stimulation. J. Neurophysiol. 8, WALL, P. D. & DAvIs, G. D. (1951). Three cerebral cortical systems affecting autonomic function. J. Neurophysiol. 14, WARD, A. A., Jr, (1948). The cingular gyrus: area 24. J. Neurophysiol. 11, PHYSIO. CXXIX
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