Adv. Cardiol., vol. IS, pp.167-175 (Karger, Base11976)

Neural Control Mechanisms Related to Physical Training T.

H. HUOPANIEMI

Institute of Physiology, University of Helsinki, Helsinki

1. Anticipatory Adjustments

A. Central Activation During somatomotor activation, some orienting adjustments in the circulation take place in anticipation to the muscular effort. In the intact organism, the impetus to respond to a new situation comes to the cardiovascular system from the cerebral cortex at the time of mental activation, when the individual feels threatened (defence reaction) or when the need for intentional motor activity rises. The impulses go through the autonomic centres of the brain stem with the final outcome of an integrated stereotypic cardiovascular response, although stimuli causing activation may vary greatly. The well-known pressor reaction includes increased cardiac output and active vasodilatation in the skeletal muscles [25]. This response is called forth within a very short time lag and it considerably overshoots the metabolic needs of the organism, thus producing cardiovascular performance ahead of the exertion [13]. The pressor reaction in man can be demonstrated while preparing for muscular work [3] and during emotional stress [2], and also in experimental animals by stimulating electrically certain areas in the hypothalamus and cerebral cortex [22] or by conditioning measures [4]. The extent of the anticipatory cardiovascular responses is in proportion to the mental engagement preceding muscular activity. It is conceivable that the autonomic nervous drive decreases due to habituation at least when smaller muscle groups are used [13]. The cerebral cortex is the major substrate in the conditioning process in which the organism learns to supply

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tachycardia, moderate blood pressure elevation, splanchnic vasoconstriction

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the proper amount of autonomic energy in association to different types of motor activity.

B. Sympathetic Cholinergic Vasodilatation

In spite of the close functional relationship of the sympathetic cholinergic vasodilatation to other circulatory changes during pressor reaction in states of alertness, no nervous connection with the classic vasomotor centers in the medulla have been demonstrated. Nor is there any evidence that the centers would modulate the active vasodilatation [26] which originates in the motor cortex. Blood flow to the dilated vascular bed becomes 3- to 4-fo1d [26] or even 6- to 7-fo1d [13], which is a good indication of the potent redistribution of blood during active vasodilatation. According to BOLME and NOVOTNY [4], the oxygen uptake increases transiently for a very short time, although UVNAS [26] noticed that the oxygen consumption even decreased. Neither was isotope clearance accelerated. It seems that the mechanism hardly has anything to do with nutritional blood flow, but it is effective in buffering increased cardiac output during pressor reaction [5]. Although the sympathetic cholinergic vasodilatation is well documented in cats and dogs, its existence in man has long been disputed. However, transient atropine sensitive vasodilatation has been reported to take place in the human arm during emotional stress and at the beginning of muscular effort [3]. The hemodynamic significance of the mechanism in man is uncertain. It may be masked in the very prompt and potent non-cholinergic vasodilatation due to autoregulation.

The mechanism of tachycardia and blood pressure elevation during emotional alertness, somatomotor activation and at the very beginning of muscular work naturally involves changes in the reciprocal balance of efferent autonomic discharges. FREYSCHUSS [14] has made a series of experiments using agents blocking the autonomic nervous system and the neuromuscular junction. Without blockade at the beginning of sustained handgrip, tachycardia and blood pressure elevation are almost immediate, elicited usually in less than 3 sec. This supports the notion that the response is of neurogenic origin. Respiratory movements or elevation of the right atrial

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C. Vagal Withdrawal

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pressure were not observed to contribute to the response. Atropinization eliminated the heart rate acceleration. The blood pressure remained high after administration of atropine, but phentolamine reduced it markedly. She concluded that the increase in heart rate was caused mainly by inhibition of the vagal tone and the elevation of blood pressure was due both to increased heart rate and a-adrenergic vasoconstriction mediated by the sympathetic nervous system. In tetraplegic patients with complete transverse spinal syndrome below CS-C7, the contraction of the forearm muscles was followed by increased heart rate. This response, which was exactly the same as in healthy individuals, took place although the patients were deprived of centrally controlled sympathetic nervous discharge to the heart. When a neuromuscular blocking drug, succinylcholine, was injected to the upper extremity intra-arterially, the attempt to contract the blocked muscles caused increased heart rate which was 64% of the appropriate control and elevation of blood pressure which was 55% of the control, although EMG revealed total absence of activity. ROBINSON et al. [21] observed that during mild exercise (oxygen uptake less than 500 ml/min) the heart rate increase was primarily associated with diminution of parasympathetic tone and at higher working intensities sympathetic activity prevailed. HOLLANDER and BOUMAN [17] measured a 550-msec time lag between the muscle contraction and the first shortening of the R-R interval. The delay and the change in heart rate were similar both when voluntary and electrically stimulated contractions were used. Cutaneous stimulation did not affect the pulse interval. The vagal inhibition of central origin seems to be a component of the mechanism preparing the cardiovascular system to respond to muscular activity. But it may also be concluded that even the first intensive muscle contraction, either intentional or electrically induced, can produce the vagal withdrawal. The response correlates with the force of the contraction but not with the muscle mass.

II. Origin of the Sympathetic Tone During Exertion

At the beginning of exercise, the prompt adaptation of the autonomic nervous system is mainly of central origin. It is, however, hard to believe that the central nervous system would have sufficient capacity to maintain

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A. Peripheral Mechanisms

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the sympathetic supply needed fOf the gradually increasing load in the cardiovascular system without reinforcing information from the periphery. The increased sympathetic activity during exercise is known to be caused by two different mechanisms: the peripheral stimulating signals are multiplied and the inhibiting reflexes become weaker. COOTE et al. [8,9] have gathered detailed information about various afferent somatic signals that on reflex level maintain the sympathetic drive. The stimulation of the spinal ventral root in unanesthetized cat caused a rise in blood pressure, which was in proportion to the tension developed in the muscle. The sectioning of the dorsal sensory root and neuromuscular blocking by gallamine both abolished the pressor response. Thus, the muscle contraction and the intact sensory nerve were necessary. When the arterial circulation to the tetanized muscle was occluded, the pressor response was potentiated. DONALD et al. [10] found pressure elevation and tachycardia during voluntary sustained handgrip. After occlusion of the forearm circulation, the pressure remained high until the cuff was released, although the contractions were stopped before. These findings strongly indicate the existence of 'metabolic receptors' sensing chemical rather than mechanical changes in their environment. The prolonged circulation after strenuous work, until the oxygen debt is repayed, also sustains this idea. COOTE et al. [8, 9] could not verify the hypothesis that mechanoreceptors in muscles are involved, and they suggested that free nerve endings fulfill the criteria of 'metabolic exercise receptors'. Their nature is, however, still unravelled. BARRON and COOTE [1] have emphasized the role of articular receptors as a source of somatosympathetic reflex.

Sciatic nerve stimulation causes a typical pressure reaction which is the result of enhanced sympathetic activity and withdrawal of cardiac vagal activity. The frequency and intensity of stimulation must be high enough, stimulation of low frequency and intensity may elicit a depressor reaction [18]. QUEST and GEBBER [20] noticed that sciatic nerve stimulation inhibited the vagal bradycardia evoked by carotid sinus nerve stimulation in dog. Inhibition of the baroreceptor reflex can also be produced by electric stimulation of posterior and lateral hypothalamus, cerebellum and the limbic area. The quantitative significance of different mechanisms influencing the sensitivity of the baroreceptor reflex is uncertain.

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B. Inhibition of the Baroreceptor Reflex

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BRISTOW et al. [6] used intravenous injections of phenylephrine, a betasympathomimetic drug, in man in order to change the baroreceptor reflex sensitivity expressed as systolic pressure-pulse interval relation. During bicycle ergometer exercise, the reflex heart rate response to artificial elevation of blood pressure decreased progressively in proportion to the work load. After the heart rate had reached the level of 150 beats/min, no reflex cardiac slowing could be demonstrated. Carotid sinus baropacing has been used in hypertensive patients in studying the sensitivity of the baroreceptor reflex. ECKBERG et at. [12] found that during treadmill exercise, heart rate response to pacer stimulation was depressed. Atropinization had no additional effect on the heart rate. Baropacing did not affect the arterial blood pressure during exercise. It is possible that only the vagal component of the baroreceptor reflex is suppressed during exertion [23]. The progressive decline of reflex sensitivity permits a sufficient elevation of heart rate in relation to increasing work load without interfering with the blood pressure.

III. Effects of Physical Training on the Nervous Control of Circulation

FRICK et al. [15] have analyzed the mechanism of training bradycardia using combined autonomic blockade. Two months' endurance training of previously sedentary subjects did not change the resting heart rate significantly, but at higher work loads heart rate reduction was manifest. The blockade with atropine and propranolol caused a 20% increase in the resting heart rate both before and after training in previously sedentary subjects, while the increment was over 40% in athletes. After the blockade, the heart rate was slower at all levels of exercise in the former group, but the change was minimal in athletes. It was concluded that physical training potentiates the parasympathetic effect on the heart at rest and reduces the sympathetic drive during exercise. ROBINSON et al. [21] made the same conclusion about the mechanism of the bradycardia caused by physical training. Since FRICK et al. [15] observed only small alterations in blood pressure, they expressed the opinion that a change in the function of the baroreceptor reflex was excluded.

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A. Autonomic Mechanism of the Training Bradycardia

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B. Physical Training and the Function of the Baroreflex The possible role of the baroreceptor reflex in control of cardiac output warrants further discussion. Exercise conditioning evokes bradycardia in two different ways: stroke volume becomes enlarged and cardiac output tends to decrease as the ability of muscles to extract oxygen is improved. How do the autonomic centers get information of the larger stroke volume? It has been suggested that atrial receptors may play a certain role in this context, although artificial changes of atrial pressure affect cardiac output only transiently. It has also been claimed that type A atrial receptors may be excitatory [16]. However, SCHMIDT et af. [24] strongly support the notion that baroreceptor reflex significantly participates in the control of cardiac output. In their studies on the relative significance of cardiac output and total peripheral resistance in maintaining blood pressure, they used dogs whose carotid sinuses were isolated and perfused separately. When the vagal nerves were intact, the forcing of the sinuses with high pressure caused a reduction in total peripheral resistance which was 3-5 times the reduction in cardiac output. After vagotomy, the relative contributions of cardiac output and total peripheral resistance were about the same. This might be interpreted so that at rest cardiac output is under the strict control of the baroreceptor reflex, but during exercise, when the reflex and especially its vagal component are inhibited, cardiac output is allowed to increase up to a certain level.

The enhancement of sympathetic drive with increasing work loads causes progressive vasoconstriction in the non-functioning tissues and venoconstriction in the capacity vessels. Venoconstriction, which is especially strong in skin, viscera and non-exercising muscles, tends to prevent unnecessary pooling of blood. The degree of vasoconstriction in resistance vessels is dependent in the number of sympathetic nerve fibers in the vessel wall of vascular bed, which is not uniform [13], and on the autoregulatory escape demanded by the basic metabolism of the tissue. The blood flow to the nonexercising tissues (especially to the splanchnic area) has an inverse linear relationship to the strenuousness of the exercise. During exertion at the level of maximal oxygen uptake, splanchnic blood flow is only one fifth of the resting value. A smaller reduction in splanchnic blood flow at a given work load is associated with improved physical fitness [7].

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C. Nervous Control of the Redistribution of Circulation

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Patients suffering from coronary heart disease or mitral stenosis often have restricted cardiac output, hyperkinetic central circulation and a very powerful constriction in splanchnic circulation. Exercise training causes remarkable relief to the vasoconstriction. The beneficial effects of training are explained by increased oxygen extraction of the muscles and perhaps by decreased pressure work of the heart because of decreased splanchnic vasoconstriction [7].

IV. Significance of the Neural Mechanisms Related to Exercise

A denervated heart is capable of augmenting cardiac output almost as much as an intact heart. DONALD et al. [11] found that after denervation, increase of heart rate was delayed and without any initial overshoot during exercise, although nearly the same maximal heart rate was reached as before denervation. At lower heart rates, larger stroke volume contributed to cardiac output according to the Starling mechanism in an exaggerated fashion. Also greater arteriovenous oxygen difference compensated partially the delayed increase in heart output. It is a common concept that catecholamines released from the adrenals during exercise might playa minor role in comparison with the accelerans nerves [13]. Dogs with cardiac neural ablation showed practically no increase in heart rate after adrenergic betareceptor blockade, and their working capacity declined drastically. This indicates that either intact nervous connections or unrestricted catecholamine release is necessary in order to achieve a certain degree of cardiovascular performance. Normally, the contribution of the catecholamine release might be delayed or masked in the pressor reaction mediated by the autonomic nervous system. It is generally held that the adaptive changes in the cardiovascular system caused by exercise training are mainly structural and biochemical by nature in the heart and other loaded tissues. Adaptation of the autonomic nervous system is secondary and it tends to harmonize the altered functioning of the cardiovascular system with the metabolic needs of the organism. References W. and COOTE, J. H.: The contribution of articular receptors to cardiovascular reflexes elicited by passive limb movement. J. Physiol., Lond. 235: 423436 (1973). BARRON,

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BERDINA, N. A.; KOLENKO, O. L.; KOTZ, I. M.; KUZNETZOV, A. P.; RODIONOV, I. M.; SAVTCHENK, A. P., and 1'HOREVSKY, V. I.: Increase in skeletal muscle performance during emotional stress in man. Circulation Res. 30: 642-650 (1972). BLAIR, D. A.; GLOVER, W., and RODDIE, I. G.: Vasomotor responses in the human arm during leg exercise. Circulation Res. 9: 264 (1961). BOLME, P. and NOVOTNY, J.: Oxygen uptake in skeletal muscle of the anesthetized dog during sympathetic vasodilatation. Acta physiol. scand. 77: 333-343 (1969). BOLME, P. and NOVOTNY, J.: Activation in the conscious dog of the sympathetic cholinergic vasodilator nerves and a proposal of their physiological significance. Acta physiol. scand. 77: suppl. 330, p. 93 (1969). BRISTOW, J. D.; BROWN, E. B., jr.; CUNNINGHAM, D. J. C.; HOWSON, M. G.; PETERSEN, E. S.; PICKERING, T. G., and SLEIGHT, P.: Effect of bicycling on the baroreflex regulation of pulse interval. Circulation Res. 28: 582-592 (1971). CLAUSEN, J. P. and TRAP-JENSEN, J.: Effects of training on the distribution of cardiac output in patients with coronary artery disease. Circulation 42: 611-624 (1970). COOTE, J. H.; HILTON, S. M., and PEREZ-GONZALES, J. F.: The reflex nature of the pressor response to muscular exercise. J. Physiol., Lond. 215: 789-804 (1971). COOTE, J. H. and PEREZ-GONZALES, J. F.: The response of some sympathetic neurones to volleys in various afferent nerves. J. Physiol., Lond. 208: 261-278 (1970). DONALD, K. W.; LIND, A. R.; McNICOL, G. W.; HUMPHREYS, S. H.; TAYLOR, S. H., and STAUNTON, H. P.: Cardiovascular responses to sustained (static) contractions. Circulation Res. 20/21: suppl. I, pp. 15-30 (1967). DONALD, D. E.; MILBURN, S. E., and SHEPHERD, J. T.: Effect of cardiac denervation on the maximal capacity for exercise in the racing greyhound. J. appl. Physiol. 19: 849-852 (1964). ECKBERG, D. L.; FLETCHER, G. F.,andBRAUNWALD, E.: Mechanism of prolongation of the R-R interval with electrical stimulation of the carotid sinus nerves in man. Circulation Res. 30: 131-138 (1972). FOLKOW, B.; HEYMANS, C., and NEIL, E.: Integrated aspects of cardiovascular regulation. Handbook of physiology, vol. 3, sec. 2, pp. 1787-1823 (American Physiological Society, Washington 1965). FREYSCHUSS, U.: Cardiovascular adjustment to somatomotor activation. Acta physiol. scand. Suppl. 342: 1-63 (1970). FRICK, M. H.; ELOVAINIO, R. 0., and SOMER, T.: The mechanism of bradycardia evoked by physical training. Cardiologia 51: 46-54 (1967). HAKUMAKI, M. O. K.: Function of the left atrial receptors. Acta physiol. scand. Suppl. 344: (1970). HOLLANDER, A. P. and BOUMAN, L. N.: Cardiac acceleration in man elicited by a muscle-heart reflex. J. appl. Physiol. 38: 272-278 (1975). JOHANSSON, B.: Circulatory responses to stimulation of somatic afferents. Acta physiol. scand. 57: suppl. 198, pp. 1-91 (1963). PEREZ-GONZALES, J. F. and COOTE, J. H.: Activity of muscle afferents and reflex circulatory responses to exercise. Am. J. Physiol. 223: 138-143 (1972). QUEST, J. A. and GERBER, G. L.: Modulation of baroreceptor reflexes by somatic afferent nerve stimulation. Am. J. Physiol. 222: 1251-1259 (1972).

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Dr. T. H. HUOPANIEMI, Institute of Physiology, University of Helsinki, Siltavuorenpenger 20a, SF-00170 Helsinki 17 (Finland)

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Neural control mechanisms related to physical training.

Adv. Cardiol., vol. IS, pp.167-175 (Karger, Base11976) Neural Control Mechanisms Related to Physical Training T. H. HUOPANIEMI Institute of Physiol...
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