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 diseases11 Mancia G, Fagard R, Narkiewicz K, Redon J, Zanchetti A, Bohm M, et al. 2013 ESH/ESC Practice Guidelines for the Management of Arterial Hypertension. Blood Press. 2014;23(1):3-16.. Increase in blood pressure is linked to neural mechanisms, e.g., autonomic dysfunction, sympathetic hyperactivity and disarray in arterial baroreceptors and chemoreceptors22. Iturriaga R, Andrade DC, Del Rio R. Crucial Role of the Carotid Body Chemo receptors on the Development of High Arterial Blood Pressure During Chronic Intermittent Hypoxia. Adv Exp Med Biol. 2015;860:255-60.,33 Smith PA, Graham LN, Mackintosh AF, Stoker JB, Mary DA. Relationship Between Central Sympathetic Activity and Stages of Human Hypertension. Am J Hypertens. 2004;17(3):217-22.,44 Chapleau MW, Li Z, Meyrelles SS, Ma X, Abboud FM. Mechanisms Determining Sensitivity of Baroreceptor Afferents in Health and Disease. Ann N Y Acad Sci. 2001;940:1-19.. The arterial baroreceptor in hypertensive subjects adapts to high levels of blood pressure, via receptors depolarization reduction, diminishing thus its functional capacity55 Consolim-Colombo FM, Fiorino P. Sistema Nervoso Simpático e Hipertensão Arterial Sistêmica: Aspectos Clínicos. Rev Bras Hiperten. 2005;12(4):251-5.,66 Krieger EM. Arterial Baroreceptor Resetting in Hypertension (the JW McCubbin memorial lecture). Clin Exp Pharmacol Physiol Suppl. 1989;15:3-17..
The role of physical exercise in blood pressure reduction has been well documented in animal models77 Kenney MJ, Seals DR. Postexercise hypotension. Key features, Mechanisms, and Clinical Significance. Hypertension. 1993;22(5):653-64. and humans88 Casonatto J, Goessler KF, Cornelissen VA, Cardoso JR, Polito MD. The blood pressure-lowering effect of a single bout of resistance exercise: A systematic review and meta-analysis of randomized controlled trials. Eur J Prev Cardiol. 2016;23(16):1700-14.,99 Marques-Silvestre ACO, Brasileiro-Santos MS, Oliveira AS, Maciel da Silva FT, Santos AC. Magnitude da Hipotensão Pós-Exercício Aeróbio Agudo: Uma Revisão Sistemática dos Estudos Randomizados. Motricidade. 2014;10(3):99-111., 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 exercise77 Kenney MJ, Seals DR. Postexercise hypotension. Key features, Mechanisms, and Clinical Significance. Hypertension. 1993;22(5):653-64..
Theautonomic mechanisms attributed to PEH are well-documented, suchas reduced peripheral sympathetic activity1010 Bisquolo VA, Cardoso CG Jr. , Ortega KC, Gusmao JL, Tinucci T, Negrao CE, et al. Previous Exercise Attenuates Muscle Sympathetic Activity and Increases Blood Flow During Acute Euglycemic Hyperinsulinemia. J Appl Physiol (1985). 2005;98(3):866-71.,1111 Halliwill JR, Taylor JA, Eckberg DL. Impaired Sympathetic Vascular Regulation in Humans After Acute Dynamic Exercise. J Physiol. 1996;495(Pt 1):279-88., modifications in the cardiac autonomic activity1212 Piepoli M, Coats AJ, Adamopoulos S, Bernardi L, Feng YH, Conway J, et al. Persistent Peripheral Vasodilation and Sympathetic Activity in Hypotension After Maximal Exercise. J Appl Physiol (1985). 1993;75(4):1807-14.,1313 Rezk CC, Marrache RC, Tinucci T, Mion D Jr., Forjaz CL. Post-Resistance Exercise Hypotension, Hemodynamics, and Heart Rate Variability: Influence of Exercise Intensity. Eur J Appl Physiol. 2006;98(1):105-12.andadjustments in the baroreflex sensitivity1414. Liu S, Goodman J, Nolan R, Lacombe S, Thomas S. Blood Pressure Responses to Acute and Chronic Exercise Are Related in Prehypertension. Med Sci Sports Exerc. 2012;44(9):1644-52.,1515 Niemela TH, Kiviniemi AM, Hautala AJ, Salmi JA, Linnamo V, Tulppo MP. Recovery Pattern of Baroreflex Sensitivity After Exercise. Med Sci Sports Exerc. 2008;40(5):864-70..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 pressure1616 Machado BH. Neurotransmission of the cardiovascular reflexes in the nucleus tractus solitarii of awake rats. Ann N Y Acad Sci. 2001;940:179-96.. Within the NTS, glutamate, a primary excitatory neurotransmitter, acts on ionotropic glutamate receptors to mediate fast synaptic transmission1717 Baude A, Strube C, Tell F, Kessler JP. Glutamatergic neurotransmission in the nucleus tractus solitarii: structural and functional characteristics. J Chem Neuroanat. 2009;38:145-53.. 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 NTS1818 Potts JT. Inhibitory neurotransmission in the nucleus tractus solitarii: implications for baroreflex resetting during exercise. Exp Physiol. 2006;91:59-72.. 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 adjustments1919 Guyenet PG. The sympathetic control of blood pressure. Nat Rev Neurosci. 2006; 7:335-46..
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 column2020 Sawchenko PE, Swanson LW. Immunohistochemical identification of neurons in the paraventricular nucleus of the hypothalamus that project to the medulla or to the spinal cord in the rat. J Comp Neurol. 1982;205:260-72., 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 pressure2121 Allen AM. Inhibition of the hypothalamic paraventricular nucleus in spontaneously hypertensive rats dramatically reduces sympathetic vasomotor tone. Hypertension 2002; 39:275-80.,2222 Badoer E. Hypothalamic paraventricular nucleus and cardiovascular regulation. Clin Exp Pharmacol Physiol. 2001;28:95-9.,2323 Strack AM, Sawyer WB, Hughes JH, Platt KB, Loewy AD. A general pattern of CNS innervation of the sympathetic outflow demonstrated by transneuronal pseudorabies viral infections. Brain Res. 1989;491:156-62..
Post-exercise hypotension
Post-exercise hypotension (PEH) has been observed in normotensive and hypertensive humans88 Casonatto J, Goessler KF, Cornelissen VA, Cardoso JR, Polito MD. The blood pressure-lowering effect of a single bout of resistance exercise: A systematic review and meta-analysis of randomized controlled trials. Eur J Prev Cardiol. 2016;23(16):1700-14.,99 Marques-Silvestre ACO, Brasileiro-Santos MS, Oliveira AS, Maciel da Silva FT, Santos AC. Magnitude da Hipotensão Pós-Exercício Aeróbio Agudo: Uma Revisão Sistemática dos Estudos Randomizados. Motricidade. 2014;10(3):99-111., likewise, in animal models of hypertension77 Kenney MJ, Seals DR. Postexercise hypotension. Key features, Mechanisms, and Clinical Significance. Hypertension. 1993;22(5):653-64., being greater in hypertensive than normotensive subjects2424 Santaella DF, Araújo EA, Ortega KC, Tinucci T, Mion Jr.D, Negrão CE, et al. After effects of exercise and relaxation on blood pressure. Clin J Sport Med (Print). 2006;16:341-7.,2525 Pescatello LS, Guidry MA, Blanchard BE, Kerr A, Taylor AL, Johnson AN, et al. Exercise intensity alters post exercise hypotension. J Hypertens. 2004;22:1881-8. ,2626 Halliwill JR. Mechanisms and clinical implications of post-exercise hypotension in humans. Exerc Sport Sci Rev. 2001;29(2):65-70. . In humans, PEH has been documented following various types of dynamic exercise (walking, running, cycling, and swimming), as well asin resistance exercise7,25,26,27,28.
The duration of PEHoccurs fromten minutes and persists until 24 hours after about of exercise2929 Ciolac EG, Guimaraes GV, D’Avila VM, Bortolotto LA, Doria EL, Bocchi EA. Acute effects of continuous and interval aerobic exercise on 24-h ambulatory blood pressure in long-term treated hypertensive patients. Int J Cardiol. 2009;133(3):381-7.,3030 Ciolac EG, Guimaraes GV, D’Avila VM, Bortolotto LA, Doria EL, Bocchi EA. Acute aerobic exercise reduces 24-h ambulatory blood pressure levels in longterm-treated hypertensive patients. Clinics (São Paulo). 2008;63(6):753-8.. Different methods have been used to assess it, such as the auscultatory method3131 Brandao Rondon MU, Alves MJ, Braga AM, Teixeira OT, Barretto AC, Krieger EM, et al. Postexercise blood pressure reduction in elderly hypertensive patients. J Am Coll Cardiol. 2002;39(4):676-82.,3232 Cunha GA, Rios ACS, Moreno JR, Braga PL, Campbell CSG, Simões HG, Denadai MLDR. Post-exercise hypotension in hypertensive individuals submitted to aerobic exercises of alternated intensities and constant intensity-exercise. Rev Bras Med Esporte. 2006;12(6):313-7., intra-arterial measurement method3333 MacDonald JR, Hogben CD, Tarnopolsky MA, MacDougall JD. Post exercise hypotension is sustained during subsequent bouts of mild exercise and simulated activities of daily living. J Hum Hypertens. 2001;15(8):567-71.,3434 MacDonald JR, Rosenfeld JM, Tarnopolsky MA, Hogben CD, Ballantyne CS, MacDougall JD. Post exercise hypotension is not mediated by the serotonergic system in borderline hypertensive individuals. J Hum Hypertens. 2002;16(1):33-9., and ambulatory blood pressure monitoring (24h assessment)2929 Ciolac EG, Guimaraes GV, D’Avila VM, Bortolotto LA, Doria EL, Bocchi EA. Acute effects of continuous and interval aerobic exercise on 24-h ambulatory blood pressure in long-term treated hypertensive patients. Int J Cardiol. 2009;133(3):381-7.,3030 Ciolac EG, Guimaraes GV, D’Avila VM, Bortolotto LA, Doria EL, Bocchi EA. Acute aerobic exercise reduces 24-h ambulatory blood pressure levels in longterm-treated hypertensive patients. Clinics (São Paulo). 2008;63(6):753-8.,3131 Brandao Rondon MU, Alves MJ, Braga AM, Teixeira OT, Barretto AC, Krieger EM, et al. Postexercise blood pressure reduction in elderly hypertensive patients. J Am Coll Cardiol. 2002;39(4):676-82.,3535 Queiroz AC, Gagliardi JF, Forjaz CL, Rezk CC. Clinic and ambulatory blood pressure responses after resistance exercise. J Strength Cond Res. 2009;23(2):571-8.. In the recent meta-analysis, Cassonatto et al.88 Casonatto J, Goessler KF, Cornelissen VA, Cardoso JR, Polito MD. The blood pressure-lowering effect of a single bout of resistance exercise: A systematic review and meta-analysis of randomized controlled trials. Eur J Prev Cardiol. 2016;23(16):1700-14.showed 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.99 Marques-Silvestre ACO, Brasileiro-Santos MS, Oliveira AS, Maciel da Silva FT, Santos AC. Magnitude da Hipotensão Pós-Exercício Aeróbio Agudo: Uma Revisão Sistemática dos Estudos Randomizados. Motricidade. 2014;10(3):99-111.found 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%3636 Lawes CM, Bennett DA, Feigin VL, Rodgers A. Bloodpressureand stroke: an overview of published reviews. Stroke. 2004;35(4):1024-33.. Also, it is interesting to note that the time and magnitude of PEH depends on thesubject’scharacteristics3737 Forjaz CLM, Tinucci T, Ortega KC, Santaella DF, Mion Jr.D, Negrão CE. Factors Affecting Post-Exercise Hypotension in Normotensive and Hypertensive Humans. Blood Press Monit. 2000;5:255-62., physical activity type3434 MacDonald JR, Rosenfeld JM, Tarnopolsky MA, Hogben CD, Ballantyne CS, MacDougall JD. Post exercise hypotension is not mediated by the serotonergic system in borderline hypertensive individuals. J Hum Hypertens. 2002;16(1):33-9.,3838 Christofaro DG, Casonatto J, Fernandes RA, Cucato GG, Gonçalves CGS, Oliveira AR, et al. Efeito da Duração do Exercício Aeróbio sobre as Respostas Hipotensivas Agudas Pós-Exercício. Rev SOCERJ. 2008;21:404-8., muscle mass involved3939 MacDonald JR, MacDougall JD, Hogben CD. The effects of exercising muscle mass on post exercise hypotension. J Hum Hypertens. 2000;14(5):317-20., duration, volume and/or intensity of physical activity performed2525 Pescatello LS, Guidry MA, Blanchard BE, Kerr A, Taylor AL, Johnson AN, et al. Exercise intensity alters post exercise hypotension. J Hypertens. 2004;22:1881-8. ,4040 Carvalho RS, Pires CM, Junqueira GC, Freitas D, Marchi-Alves LM. Hypotensive response magnitude and duration in hypertensives: continuous and interval exercise. Arq Bras Cardiol. 2015;104(3):234-41. ,4141 Mach C, Foster C, Brice G, Mikat RP, Porcari JP. Effect of exercise duration on postexercise hypotension. J Cardiopulm Rehabil. 2005;25:366-9. ,4242 Forjaz CL, Cardoso CG Jr, Rezk CC, Santaella DF, Tinucci T. Postexercise Hypotension and Hemodynamics: The Role of Exercise Intensity. J Sports Med Phys Fitness. 2004;44(1):54-62..
The use of physical exercise to reduce blood pressure in hypertensive subjects is already well emphasized in clinical trials and systematic reviews88 Casonatto J, Goessler KF, Cornelissen VA, Cardoso JR, Polito MD. The blood pressure-lowering effect of a single bout of resistance exercise: A systematic review and meta-analysis of randomized controlled trials. Eur J Prev Cardiol. 2016;23(16):1700-14.,4343 Cardoso Jr CG. , Gomides RS, Queiroz AC, Pinto LG, Silveira Lobo F, Tinucci T, et al. Acute and Chronic Effects of Aerobic and Resistance Exercise on Ambulatory Blood Pressure. Clinics. 2010;65(3):317-25.,4444 Mota MR, Pardono E, Lima LC, Arsa G, Bottaro M, Campbell CS, et al. Effects of Treadmill Running and Resistance Exercises on Lowering Blood Pressure During the Daily Work of Hypertensive Subjects. J Strength Cond Res. 2009;23(8):2331-8.,4545 Moraes MR, Bacurau RF, Ramalho JD, Reis FC, Casarini DE, Chagas JR, et al. Increase in Kinins on Post-Exercise Hypotension in Normotensive and Hypertensive Volunteers. Biol Chem. 2007;388(5):533-40.. In addition, several clinical trials identified the effectiveness of physical training to reduce blood pressure levels4646 Laterza MC, Matos LD, Trombetta IC, Braga AM, Roveda F, Alves MJ, et al. Exercise Training Restores Baroreflex Sensitivity in Never-Treated Hypertensive Patients. Hypertension. 2007;49(6):1298-306.,4747 Pinto A, Di Raimondo D, Tuttolomondo A, Fernandez P, Arnao V, Licata G. Twenty-four Hour Ambulatory Blood Pressure Monitoring to Evaluate Effects on Blood Pressure of Physical Activity in Hypertensive Patients. Clin J Sport Med. 2006;16(3):238-43.,4848 Syme AN, Blanchard BE, Guidry MA, Taylor AW, Vanheest JL, Hasson S, et al. Peak Systolic Blood Pressure on a Graded Maximal Exercise Test and the Blood Pressure Response to an Acute Bout of Submaximal Exercise. Am J Cardiol. 2006;98(7):938-43., as well as in meta-analysis77 Kenney MJ, Seals DR. Postexercise hypotension. Key features, Mechanisms, and Clinical Significance. Hypertension. 1993;22(5):653-64.,4949 Fagard RH. Exercise is Good for Your Blood Pressure: Effects of Endurance Training and Resistance Training. Clin Exp Pharmacol Physiol. 2006;33(9):853-6.,5050 Whelton SP, Chin A, Xin X, He J. Effect of aerobic exercise on blood pressure: a meta analysis of randomized, controlled trials. Ann Intern Med Ann Intern Med. 2002; 136(7):493-503. ,5151 Halbert JA, Silagy CA, Finucane P, Withers RT, Hamdorf PA, Andrews GR. The Effectiveness of Exercise Training in Lowering Blood Pressure: A Meta-Analysis of Randomised Controlled Trials of 4 Weeks or Longer. J Hum Hypertens.1997;11(10):641-9.. Meta-analysis of Halbert et al.5151 Halbert JA, Silagy CA, Finucane P, Withers RT, Hamdorf PA, Andrews GR. The Effectiveness of Exercise Training in Lowering Blood Pressure: A Meta-Analysis of Randomised Controlled Trials of 4 Weeks or Longer. J Hum Hypertens.1997;11(10):641-9.published for two decades, showed reductions of -4.7mmHg and -3.1mmHg insystolic and diastolic blood pressure, respectively. Fagard4949 Fagard RH. Exercise is Good for Your Blood Pressure: Effects of Endurance Training and Resistance Training. Clin Exp Pharmacol Physiol. 2006;33(9):853-6.identifiedreductions of -3.3 mmHg insystolic blood pressure and -3.5 mmHg indiastolic blood pressure. Similarly,Whelton et al.5050 Whelton SP, Chin A, Xin X, He J. Effect of aerobic exercise on blood pressure: a meta analysis of randomized, controlled trials. Ann Intern Med Ann Intern Med. 2002; 136(7):493-503. 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 sensitivity1010 Bisquolo VA, Cardoso CG Jr. , Ortega KC, Gusmao JL, Tinucci T, Negrao CE, et al. Previous Exercise Attenuates Muscle Sympathetic Activity and Increases Blood Flow During Acute Euglycemic Hyperinsulinemia. J Appl Physiol (1985). 2005;98(3):866-71.,1111 Halliwill JR, Taylor JA, Eckberg DL. Impaired Sympathetic Vascular Regulation in Humans After Acute Dynamic Exercise. J Physiol. 1996;495(Pt 1):279-88.,2626 Halliwill JR. Mechanisms and clinical implications of post-exercise hypotension in humans. Exerc Sport Sci Rev. 2001;29(2):65-70. ,4646 Laterza MC, Matos LD, Trombetta IC, Braga AM, Roveda F, Alves MJ, et al. Exercise Training Restores Baroreflex Sensitivity in Never-Treated Hypertensive Patients. Hypertension. 2007;49(6):1298-306..In table 1 are presented post-exercise autonomic responses assessed by different methods. Overall, there were reductions of muscle sympathetic nerve activity after aerobic exercise1010 Bisquolo VA, Cardoso CG Jr. , Ortega KC, Gusmao JL, Tinucci T, Negrao CE, et al. Previous Exercise Attenuates Muscle Sympathetic Activity and Increases Blood Flow During Acute Euglycemic Hyperinsulinemia. J Appl Physiol (1985). 2005;98(3):866-71.,1111 Halliwill JR, Taylor JA, Eckberg DL. Impaired Sympathetic Vascular Regulation in Humans After Acute Dynamic Exercise. J Physiol. 1996;495(Pt 1):279-88.,5252 Aprile DC, Oneda B, Gusmão JL, Costa LA, Forjaz CL, Mion D Jr, et al. Post-Exercise Hypotension Is Mediated by a Decrease in Sympathetic Nerve Activity in Stages 2-3 CKD. Am J Nephrol. 2016;43(3):206-12. , reduction of cardiac autonomic balance1414. Liu S, Goodman J, Nolan R, Lacombe S, Thomas S. Blood Pressure Responses to Acute and Chronic Exercise Are Related in Prehypertension. Med Sci Sports Exerc. 2012;44(9):1644-52.,5353. Trevizani GA, Peçanha T, Nasario-Junior O, Vianna JM, Silva LP, Nadal J. Cardiac autonomic responses after resistance exercise in treated hypertensive subjects. Front Physiol. 2015;6:1-7., and increase of baroreflex sensitivity and heart rate variability5454 Raczak G, Pinna GD, La Rovere MT, Maestri R, Danilowicz-Szymanowicz L, Ratkowski W, et al. Cardiovagal response to acute mild exercise in young healthy subjects. Circ J. 2005;69(8):976-80.. Contrarily, other studies reported increased cardiac and vasomotor sympathetic modulation, decreased parasympathetic modulation and/orattenuation of baroreflex sensitivity1212 Piepoli M, Coats AJ, Adamopoulos S, Bernardi L, Feng YH, Conway J, et al. Persistent Peripheral Vasodilation and Sympathetic Activity in Hypotension After Maximal Exercise. J Appl Physiol (1985). 1993;75(4):1807-14.,1313 Rezk CC, Marrache RC, Tinucci T, Mion D Jr., Forjaz CL. Post-Resistance Exercise Hypotension, Hemodynamics, and Heart Rate Variability: Influence of Exercise Intensity. Eur J Appl Physiol. 2006;98(1):105-12.,1515 Niemela TH, Kiviniemi AM, Hautala AJ, Salmi JA, Linnamo V, Tulppo MP. Recovery Pattern of Baroreflex Sensitivity After Exercise. Med Sci Sports Exerc. 2008;40(5):864-70.,5555 Queiroz ACC, Sousa JCS, Cavalli AAP, Silva Jr ND, Costa LAR,Tobaldini E, et al. Post-resistance exercise hemodynamic and autonomic responses: Comparison between normotensive and hypertensive men. Scand J Med Sci Sports. 2015;25:486-94. however, those studies used resistance exercise1313 Rezk CC, Marrache RC, Tinucci T, Mion D Jr., Forjaz CL. Post-Resistance Exercise Hypotension, Hemodynamics, and Heart Rate Variability: Influence of Exercise Intensity. Eur J Appl Physiol. 2006;98(1):105-12.,1515 Niemela TH, Kiviniemi AM, Hautala AJ, Salmi JA, Linnamo V, Tulppo MP. Recovery Pattern of Baroreflex Sensitivity After Exercise. Med Sci Sports Exerc. 2008;40(5):864-70.,5555 Queiroz ACC, Sousa JCS, Cavalli AAP, Silva Jr ND, Costa LAR,Tobaldini E, et al. Post-resistance exercise hemodynamic and autonomic responses: Comparison between normotensive and hypertensive men. Scand J Med Sci Sports. 2015;25:486-94.or maximal aerobic exercise1212 Piepoli M, Coats AJ, Adamopoulos S, Bernardi L, Feng YH, Conway J, et al. Persistent Peripheral Vasodilation and Sympathetic Activity in Hypotension After Maximal Exercise. J Appl Physiol (1985). 1993;75(4):1807-14..
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 RVLM5656 Mueller PJ. Exercise training attenuates increases in lumbar sympathetic nerve activity produced by stimulation of the rostral ventrolateral medulla. J Appl Physiol. 2007;102:803-13.,5757 Martins-Pinge MC, Becker LK, Garcia MR, Zoccal DB, Neto RV, Basso LS, et al. Attenuated pressor responses to amino acids in the rostral ventrolateral medulla after swimming training in conscious rats. Auton Neurosci. 2005;122:21-8. , NTS5858 Michelini LC, Stern JE. Exercise-induced neuronal plasticity in central autonomic networks: role in cardiovascular control. Exp Physiol. 2009; 94:947-60.,5959 De Souza CG, Michelini LC, Fior-Chadi DR. Receptor changes in the nucleus tractus solitarii of the rat after exercise training. Med Sci Sports Exerc. 2001;33:1471-6., and PVN5858 Michelini LC, Stern JE. Exercise-induced neuronal plasticity in central autonomic networks: role in cardiovascular control. Exp Physiol. 2009; 94:947-60.,6060 Mastelari RB, de Souza HC, Lenhard A, de Aguiar Correa FM, Martins-Pinge MC. Nitric oxide inhibition in paraventricular nucleus on cardiovascular and autonomic modulation after exercise training in unanesthetized rats. Brain Res. 2011;1375:68-76.,6161 de Abreu SB, Lenhard A, Mehanna A, de Souza HC, Correa FM, Hasser EM, et al. Role of paraventricular nucleus in exercise training-induced autonomic modulation in conscious rats. Auton Neurosci. 2009;148:28-35. 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. Corry6262 Boone JB Jr, Corry JM. Proenkephalin gene expression in the brainstem regulates post-exercise hypotension. Brain Res Mol Brain Res. 1996;42:31-8. 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 SHR6363. Shyu BC, Thorén P. Circulatory events following spontaneous muscle exercise in normotensive and hypertensive rats. Acta Physiol Scand. 1986;128:515-24.. In addition, injections of vasopressin V1 receptor antagonist into the lateral cerebral ventricle impedes the manifestation of PEH6464 Collins HL, Rodenbaugh DW, DiCarlo SE. Central blockade of vasopressin V(1) receptors attenuates postexercise hypotension. Am J Physiol Regul Integr Comp Physiol. 2001;281:R375-80.. 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.
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 PEH6565 Collins HL, DiCarlo SE. Attenuation of postexertional hypotension by cardiac afferent blockade. Am J Physiol. 1993;265:H1179-83.. Correspondingly, Chandler and DiCarlo6666 Chandler MP, DiCarlo SE. Sinoaortic denervation prevents postexercise reductions in arterial pressure and cardiac sympathetic tonus. Am J Physiol. 1997;273:H2738-45. 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 exercise6767 Kulics JM, Collins HL, DiCarlo SE. Postexercise hypotension is mediated by reductions in sympathetic nerve activity. Am J Physiol Heart Circ Physio. 1999;276(1):H27-32., 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.6868 Kajekar R, Chen CY, Mutoh T, Bonham AC. GABA(A) receptor activation at medullary sympathetic neurons contributes to postexercise hypotension. Am J Physiol Heart Circ Physiol. 2002;282:H1615-24.brilliantly 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 exercise2121 Allen AM. Inhibition of the hypothalamic paraventricular nucleus in spontaneously hypertensive rats dramatically reduces sympathetic vasomotor tone. Hypertension 2002; 39:275-80.,6969 Boscan P, Paton JF.Excitatory convergence of periaqueductal gray and somatic afferents in the solitary tract nucleus: role for neurokinin 1 receptors. Am J Physiol Regul Integr Comp Physiol. 2005;288:R262-69.,7070 Potts JT, Fuchs IE, Li J, Leshnower B, Mitchell JH. Skeletal muscle afferent fibres release substance P in the nucleus tractus solitarii of anaesthetized cats. J Physiol. 1999; 514:829-41. . 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.7171 Chen CY, Munch PA, Quail AW, Bonham AC. Postexercise hypotension in conscious SHR is attenuated by blockade of substance P receptors in NTS. Am J Physiol Heart Circ Physiol. 2002; 283:H1856-62.inan 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 internalization7272 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., 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.7373. Chen CY, Bechtold AG, Tabor J, Bonham AC. Exercise reduces GABA synaptic input onto nucleus tractus solitarii baroreceptor second-order neurons via NK1 receptor internalization in spontaneously hypertensive rats. J Neurosci. 2009;29:2754-61.proposed 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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65Collins HL, DiCarlo SE. Attenuation of postexertional hypotension by cardiac afferent blockade. Am J Physiol. 1993;265:H1179-83.
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66Chandler MP, DiCarlo SE. Sinoaortic denervation prevents postexercise reductions in arterial pressure and cardiac sympathetic tonus. Am J Physiol. 1997;273:H2738-45.
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67Kulics JM, Collins HL, DiCarlo SE. Postexercise hypotension is mediated by reductions in sympathetic nerve activity. Am J Physiol Heart Circ Physio. 1999;276(1):H27-32.
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68Kajekar R, Chen CY, Mutoh T, Bonham AC. GABA(A) receptor activation at medullary sympathetic neurons contributes to postexercise hypotension. Am J Physiol Heart Circ Physiol. 2002;282:H1615-24.
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69Boscan P, Paton JF.Excitatory convergence of periaqueductal gray and somatic afferents in the solitary tract nucleus: role for neurokinin 1 receptors. Am J Physiol Regul Integr Comp Physiol. 2005;288:R262-69.
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70Potts JT, Fuchs IE, Li J, Leshnower B, Mitchell JH. Skeletal muscle afferent fibres release substance P in the nucleus tractus solitarii of anaesthetized cats. J Physiol. 1999; 514:829-41.
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71Chen CY, Munch PA, Quail AW, Bonham AC. Postexercise hypotension in conscious SHR is attenuated by blockade of substance P receptors in NTS. Am J Physiol Heart Circ Physiol. 2002; 283:H1856-62.
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72Marvizón 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.
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Publication Dates
-
Publication in this collection
2017
History
-
Received
15 Sept 2016 -
Accepted
01 Nov 2016