Neural mechanismsand post-exercise hypotension: The importance of experimental studies

Abstract

A single bout of exercise can decrease blood pressure level in hypertensive individuals and this phenomenon is known as post-exercise hypotension (PEH). PEH is clinically important and reduces blood pressure after physical exercise in hypertensive subjects. This reduction has been attributed to autonomic mechanisms, e.g., reduced peripheral sympathetic activity, adjustments in cardiac autonomic balance and baroreflex sensitivity. Besides, evidence has suggested that the central baroreflex pathway has an important role in the occurrence of PEH. Therefore, the aim of this study was to review the effects of physical exercise on areas of the central nervous system involved in the regulation of blood pressure.

Keywords
central nervous system; post-exercise hypotension; mechanisms

Introduction

Systemic hypertension is a multifactorial clinical condition and an independent risk factor for mortality inpatients with cardiovascular diseases¹. Increase in blood pressure is linked to neural mechanisms, e.g., autonomic dysfunction, sympathetic hyperactivity and disarray in arterial baroreceptors and chemoreceptors²,³,⁴. The arterial baroreceptor in hypertensive subjects adapts to high levels of blood pressure, via receptors depolarization reduction, diminishing thus its functional capacity⁵,⁶.

The role of physical exercise in blood pressure reduction has been well documented in animal models⁷ and humans⁸,⁹, and this phenomenon occurs due to adjustments in the neurohumoral mechanisms. Post-exercise hypotension [PEH] is a prolonged decrease in arterial blood pressure after a single bout of exercise⁷.

Theautonomic mechanisms attributed to PEH are well-documented, suchas reduced peripheral sympathetic activity¹⁰,¹¹, modifications in the cardiac autonomic activity¹²,¹³andadjustments in the baroreflex sensitivity¹⁴,¹⁵.On the other hand, the central neural mechanisms have only recently been discovered and investigated. This review emphasizes on evidence of synaptic mechanisms in the central baroreflex pathway that contribute to development of PEH. Therefore, we will summarize studies that define important areas of central nervous system (CNS) involved in physical activities and blood pressure regulation.

Central baroreflex arc, blood pressure, and sympathetic activity

Regulation of the cardiovascular system by the baroreflex involves multiple components of the baroreflex arc, such as sensors (baroceptors), afferentspathway (depressor nerve aortic), central circuit (nucleus tractus solitarii (NTS) and others brain areas), and efferentpathway (heart, vessels). The afferent fibers baroreceptor, which carries blood pressure information, makes an excitatory synaptic contact with second-order neurons in the NTS. The NTS integrates and receives information from arterials baroceptorsand through connections with caudal ventral lateral medulla (CVLM), rostral ventral lateral medulla (RVLM), and dorsal nucleus of the vagusnerve promotes the control of hemodynamics to adjustblood pressure¹⁶. Within the NTS, glutamate, a primary excitatory neurotransmitter, acts on ionotropic glutamate receptors to mediate fast synaptic transmission¹⁷. The afferent fibers from skeletal muscle also project the NTS through a poly-synapse pathway. These ascending fibers, which carry information from the muscles, make an excitatory synapse releasing the substance P closer to the GABAergic interneurons in the NTS¹⁸. The NTS output neurons convey signals from the baroreceptors andmusclesafferent to neurons in the CVLM via excitatory glutamatergic synapses. The neuronal output of the CVLM provides inhibitory (GABAergic) inputs to the cardiovascular sympathetic neurons in the RVLM, projecting to the sympathetic pre-ganglionic neurons in the intermedio lateral cell column in the spinal cord. Therefore, increase in blood pressure activate the baroreceptors, which increases NTS neuronal activity, increasing GABA ergic neuronal activity in the CVLM, which decreases neurons activityof the RVLM and reduces the sympathetic nerve activity that returns blood pressure to the control level.

Blood pressure is determined by product of vascular peripheral resistance with cardiac output, and efferent pathways of sympathetic vasomotor outflow control both determinants factors. This sympathetic out flow presents tonic activity and has source in intermedio lateral cell column in preganglionic neurons located in the spinal cord. Moreover, this sympathetic tone activity controls the cardiovascular function through vasoconstrictors and cardio accelerator adjustments¹⁹.

Direct projections of the intermediolateral column originates predominantly from at least five areas of the brain: a) rostral ventrolateral medulla (RVLM); b) rostral ventromedial medulla;c) caudal raphe nuclei;d) A5 cell group in the pons; and e) paraventricular nucleus of the hypothalamus (PVN).The RVLM has a great relevance in sympathetic regulation to the cardiovascular system and PVN may provide a tonic excitatory drive to the RVLM neurons. PVN neurons send direct projections to sympathetic preganglionic neurons of the intermediolateral column²⁰, therefore, PNV neurons can affect the sympathetic tonus through its direct and indirect connections. Consequently, both RVLM and PVN could adjust sympathetic vasomotor tone and regulates blood pressure²¹,²²,²³.

Post-exercise hypotension

Post-exercise hypotension (PEH) has been observed in normotensive and hypertensive humans⁸,⁹, likewise, in animal models of hypertension⁷, being greater in hypertensive than normotensive subjects²⁴,²⁵,²⁶. In humans, PEH has been documented following various types of dynamic exercise (walking, running, cycling, and swimming), as well asin resistance exercise^{7,25,26,27,28}.

The duration of PEHoccurs fromten minutes and persists until 24 hours after about of exercise²⁹,³⁰. Different methods have been used to assess it, such as the auscultatory method³¹,³², intra-arterial measurement method³³,³⁴, and ambulatory blood pressure monitoring (24h assessment)²⁹,³⁰,³¹,³⁵. In the recent meta-analysis, Cassonatto et al.⁸showed that a single bout of resistance exercise elicited small-to-moderate reductions in systolic blood pressure at 60 and 90 minutes after exercise, and in 24-hour ambulatory blood pressurecompared to control session. They concluded that a single bout of resistance exercise could have a blood pressure-lowering effect that lasts up to 24 hours. Marques-Silvestre et al.⁹found in their systematic review, relevant reductions of systolic/diastolic blood pressureafter a session of dynamic aerobic exercise and it was maintained for several hours. Therefore, these post-exercise blood pressure reductions could have an impact oncardiovascular health, since a 5 mm Hg reduction is clinically significant and is associated with risk reduction for stroke and heart disease of 15%-20%³⁶. Also, it is interesting to note that the time and magnitude of PEH depends on thesubject’scharacteristics³⁷, physical activity type³⁴,³⁸, muscle mass involved³⁹, duration, volume and/or intensity of physical activity performed²⁵,⁴⁰,⁴¹,⁴².

The use of physical exercise to reduce blood pressure in hypertensive subjects is already well emphasized in clinical trials and systematic reviews⁸,⁴³,⁴⁴,⁴⁵. In addition, several clinical trials identified the effectiveness of physical training to reduce blood pressure levels⁴⁶,⁴⁷,⁴⁸, as well as in meta-analysis⁷,⁴⁹,⁵⁰,⁵¹. Meta-analysis of Halbert et al.⁵¹published for two decades, showed reductions of -4.7mmHg and -3.1mmHg insystolic and diastolic blood pressure, respectively. Fagard⁴⁹identifiedreductions of -3.3 mmHg insystolic blood pressure and -3.5 mmHg indiastolic blood pressure. Similarly,Whelton et al.⁵⁰ observed a significant reduction in systolic and diastolic blood pressure of -3.84 mmHg and -2.58 mmHg, respectively.

It is known that neural mechanisms are associatedwith PEH, such asreduction of sympathetic nervous activity, increase of vagal modulation, and improvedbaroreflex sensitivity¹⁰,¹¹,²⁶,⁴⁶.In table 1 are presented post-exercise autonomic responses assessed by different methods. Overall, there were reductions of muscle sympathetic nerve activity after aerobic exercise¹⁰,¹¹,⁵², reduction of cardiac autonomic balance¹⁴,⁵³, and increase of baroreflex sensitivity and heart rate variability⁵⁴. Contrarily, other studies reported increased cardiac and vasomotor sympathetic modulation, decreased parasympathetic modulation and/orattenuation of baroreflex sensitivity¹²,¹³,¹⁵,⁵⁵ however, those studies used resistance exercise¹³,¹⁵,⁵⁵or maximal aerobic exercise¹².

Table 1
The effect of physical exercise on autonomic and hemodynamic parameters

• ^{Abbreviations}
  SBP, systolic arterial pressure; DBP, diastolic arterial pressure; MBP, mean arterial pressure; MSNA, muscle sympathetic nerve activity; TPR, total peripheral resistance; CO, cardiac output; VO2peak, peak oxygen uptake; VO2max, maximum oxygen consumption; FVR, forearm vascular resistance; FBF, forearm blood flow; SV, stroke volume; SVR, systemic vascular resistance; BS, baroreflex sensitivity; SM, sympathetic modulation; PM, parasympathetic modulation; AB, autonomic balance; RM, repetition maximum; BRSLF, baroreflex sensitivity of low frequency band; SM-SAP, sympathetic modulation of systolic arterial pressure; SDNN, standard deviation of normal-to-normal RR intervals; HRV, heart rate variability; pNN50, duration higher than 50 ms in relation to the total number of normal-to-normal RR intervals; RMSSD, square root of the mean square differences of successive normal-to-normal RR intervals; ↓ decrease; ↔ no change; ↑ increase.

Neural mechanisms and PEH

The hemodynamic changes induced by physical exercise depends on cardiovascular autonomic activity and CNS. Regarding the areas of CNS, studies have shown that the RVLM⁵⁶,⁵⁷, NTS⁵⁸,⁵⁹, and PVN⁵⁸,⁶⁰,⁶¹ are involved with this cardiovascular control.

Evidence has shown that there are important mechanisms working in the nervous system to adjust the PEH. Table 2 shows studies that investigated the contribution of this nervous system to the occurrence of PEH. Boone and Jr. Corry⁶² demonstrated that the expression of the gene preproenkephalin (PPK) increases in the CNS after treadmill exercise in SHRs, suggesting that increase in PPK synthesis and release in the NTS, CVLM, and RVLM may be involved in regulating PEH. Previous studies on both humans and SHRs indicate that endorphin systems (opioid receptor antagonist, naloxone) attenuate PEH, and they trigger the transient depression of blood pressure immediately after running period in the SHR⁶³. In addition, injections of vasopressin V1 receptor antagonist into the lateral cerebral ventricle impedes the manifestation of PEH⁶⁴. This result supports the participation of central mechanisms in the development of PEH, even though the exact role of each receptor system and the specific site of interaction are still indeterminate.

Table 2
Experimental studies and neural mechanisms associated with PEH.

• ^{Abbreviations}
  AP, arterial pressure; PEH, post-exercise hypotension; NTS, nucleus tractus solitarii; CVLM, caudal ventrolateral medulla; RVLM, rostral ventrolateral medulla; MAP, mean arterial pressure; min, minutes; SHR, spontaneously hypertensive rats; WKY, Wistar Kyoto; SAD, sinoaortic-denervated; CO, cardiac output; TPR, total peripheral resistance; LSNA, lumbar sympathetic nervous activity; AVP, arginine vasopressin.

On the other hand, there is evidence suggesting crucial role of the central baroreflex pathway in PEH. Disturbance of inputs from the cardiopulmonary and arterial baroreflex to the CNS prior to exercise attenuates the development of PEH. Blocking the cardiac afferents and efferent fibers with intrapericardial procainamide prevents PEH⁶⁵. Correspondingly, Chandler and DiCarlo⁶⁶ observed that sinoaortic denervation, which eliminates arterial baroreflex afferents, participates in development of PEH in SHRs.These authors postulated that probably an enhanced inhibitory influence of cardiopulmonary afferents might alter the arterial baroreflex by modulating the response of barosensitive neurons in the NTS to arterial baroreceptor input. These alterations, through resetting of the arterial baroreflex with a reduction in gain, would account for the hypotension, sympatho inhibition, and absence of reflex tachycardia that occurs after a single bout of dynamic exercise in hypertensive rats. Therefore, this data has demonstrated the importance of a functioning baroreflex for occurrence of PEH. Previous investigations have shown reduction of sympathetic nerve activity after exercise⁶⁷, as might be expected during the lower blood pressure and the baroreflex-mediated regulation of the sympathetic nerve activity must be reset to a lower operating point during PEH.

In the same way, the fundamental role of the RVLM neuron sin controlling sympathetic vasomotor tone and blood pressure, the regulatory role of GABA in controlling baseline activity of those neurons and reduced baroreflex function during PEH. Thus, Kajekar et al.⁶⁸brilliantly suggested evaluating the role of RVLM cardiovascular sympathetic neuronal activity with PEH, as well as the relationship between RVLM sympathetic output with RVLM GABAA-receptor mechanisms, and with baroreflex sympathetic nerve activity. They concluded that up regulation of GABA signaling at sympathetic cardiovascular RVLM neurons lead to a decreased neuronal output that may contribute to the decrease in sympathetic out flow and hence PEH. Several evidences suggest that muscle afferent fibers release the substance P to activate NK1-R on GABA neurons in the NTS to modify baroreflex function during exercise²¹,⁶⁹,⁷⁰. The data raised the possibility that the unique interaction between the substance P and GABA ergic signal transmission systems may contribute to PEH. Based on this information, Chen et al.⁷¹inan elegant study confirmed that microinjection of a substance P-NK1-R antagonist in the NTS immediately before exercise attenuates the development of PEH in spontaneously hypertensive rats (SHRs). Since that activation of the NK1-R has been shown to result in the receptor internalization⁷², exercise-induced substance P NK1-R internalization on GABA neurons may provide the unique interaction between the two neurotransmission systems to trigger PEH. Later, Chen et al.⁷³proposed testing the hypothesis of how a single bout of dynamic exercise decreases the GABA inhibitory synaptic inputs in the NTS baroreceptor second-order neurons via substance P NK1-R internalization on GABA neurons in SHRs, and evidence that a decrease in blood pressure induced by a single bout of exercise in hypertension is mediated in part by down regulation of NK1-R on GABA neurons synapsing on NTS second-order baroreceptor neurons. They concluded that a single bout of dynamic exercise decreases the GABA inhibitory synaptic inputs in the NTS baroreceptor second-order neurons via substance P NK1-R internalization on GABA neurons, and suggest that exercise-induced NK1-R down regulation could provide a potential target for lowering blood pressure in hypertensive subjects.

Considerations

The paraventricular nucleus of the hypothalamus (PVN) and the rostral ventrolateral medulla (RVLM) promotes tonic effect on the control of sympathetic vasomotor tone that triggers blood pressure responses. Thus, there are evidences on baroreflex system and central mechanisms related to PEH. The main central mechanisms are(1)interaction between substance P and the GABAergic system in the NTS that contributes to PEH, and (2) baroreceptor neurons disinhibited in the NTS increases RVLM inhibition, via activation of the GABAergic neurons in the CVLM, reduces PEH. We concluded that the nervous system has an important contribution to reduce post exercise blood pressure. In addition, the baroreflex system is important to adjust PEH, as well as nucleus tractus solitarii and RVLM involvement is fundament alto its occurrence.

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  Marvizón JC, Wang X, Matsuka Y, Neubert JK, Spigelman I. Relationship between capsaicin-evoked substance P release and neurokinin 1 receptor internalization in the rat spinal cord. Neuroscience. 2003;118:535-45.
• ⁷³
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Publication Dates

• Publication in this collection
  2017

History

• Received
  15 Sept 2016
• Accepted
  01 Nov 2016