Russian Journal of PhysiologyRussian Journal of PhysiologyРоссийский физиологический журнал им. И.М. Сеченова0869-81392658-655XThe Russian Academy of Sciences65168310.31857/S0869813924010053WQDMTFEXPERIMENTAL ARTICLESЭКСПЕРИМЕНТАЛЬНЫЕ СТАТЬИResearch ArticleThe change in Baroreflex Regulation of Heart Rhythm after “Dry” Immersion Appears during Orthostasis, but not Lower Body Negative Pressure TestИзменение барорефлекторной регуляции ритма сердца после “сухой” иммерсии проявляется при ортостазе, но не при отрицательном давлении на нижнюю часть телаZhedyaevR. Yu.ЖедяевР. Ю.
Russian Federation
zhedyaev-r@mail.ruTarasovaO. S.ТарасоваО. С.
Russian Federation
zhedyaev-r@mail.ruSemenovYu. S.СеменовЮ. С.
Russian Federation
zhedyaev-r@mail.ruBorovikA. S.БоровикА. С.
Russian Federation
zhedyaev-r@mail.ruVinogradovaO. L.ВиноградоваО. Л.
Russian Federation
zhedyaev-r@mail.ruInstitute of Biomedical Problems, Russian Academy of SciencesИнститут медико-биологических проблем РАНLomonosov Moscow State UniversityМосковский государственный университет имени М.В. Ломоносова150120241101799301022025Copyright ©; 2024, Russian Academy of SciencesCopyright ©; 2024, Российская академия наук2024Russian Academy of SciencesРоссийская академия наукhttps://journals.eco-vector.com/0869-8139/article/view/651683

The ratio of low-frequency (LF, ~0.1 Hz) waves of RR interval duration (RRI) and systolic blood pressure (SAP) reflects the cardiac baroreflex sensitivity (BRS). Gravitational unloading (GU) may alter BRS during the passive orthostatic test (HUT) and lower body negative pressure (LBNP) test. Both effects cause blood redistribution to the lower body, but HUT is accompanied by greater unloading of sinocarotid baroreceptors than LBNP and activation of the vestibulosympathetic reflex but GU effects on BRS in these tests have not been directly compared previously. In this study we tested the hypothesis that the effect of “dry” immersion (DI, on-ground model of GU) on BRS in the same subjects will be more pronounced during HUT than during LBNP, which causes a comparable decrease in stroke volume. Nine healthy men participated in two test sessions (before and after 7-day DI) consisting of five 3-min HUT (65°) and five 3-min LBNP (–35 mmHg) with averaging the parameters in each test. Wavelet analysis was used to determine the amplitude of the RRI and SAP waves in the range of 0.05–0.13 Hz. The amplitude of LF waves of SAP increased in both tests, after DI - more significantly in HUT. The amplitude of LF RRI waves decreased in the two tests; the degree of decrease did not differ between tests and did not change under the influence of DI. The α-coefficient (the ratio of the amplitudes of RRI and SAP LF waves) decreased equally in the two tests before DI, but after DI, the degree of α-coefficient reduction increased in HUT test but did not change in LBNP test. Thus, the effect of DI on BRS is evident in HUT, but not in LBNP, which may be explained by the more pronounced influence of HUT on the mechanisms of neural control of heart rhythm.

Соотношение низкочастотных (~0.1 Гц) волн длительности RR-интервала и систолического артериального давления (АД) отражает чувствительность кардиохронотропного барорефлекса. Гравитационная разгрузка может приводить к изменению чувствительности кардиохронотропного барорефлекса во время пассивного ортостатического теста (ОТ) и теста с созданием отрицательного давления на нижнюю часть тела (ОДНТ). Оба воздействия вызывают перераспределение крови в нижнюю часть тела, но ОТ сопровождается большей разгрузкой синокаротидных барорецепторов, по сравнению с ОДНТ, и активацией вестибулосимпатического рефлекса, однако прямого сопоставления эффектов гравитационной разгрузки на чувствительность кардиохронотропного барорефлекса в этих тестах ранее не проводилось. Целью данной работы была проверка гипотезы о том, что влияние “сухой” иммерсии (наземная модель гравитационной разгрузки) на чувствительность кардиохронотропного барорефлекса у одних и тех же испытуемых будет ярче проявляться при ОТ, чем при ОДНТ, вызывающем сопоставимое по величине снижение ударного объема. Девять здоровых мужчин участвовали в двух тестированиях (до и после 7-дневной сухой иммерсии), включавших по пять 3-минутных ОТ (65°) и пять 3-минутных тестов ОДНТ (–35 мм рт. ст.) с последующим усреднением показателей для каждого воздействия. Амплитуду низкочастотных волн RR-интервала и систолического АД в диапазоне 0.05–0.13 Гц определяли с помощью вейвлет-анализа. Амплитуда низкочастотных волн систолического АД увеличивалась в обоих тестах, после гравитационной разгрузки – сильнее при ОТ. Амплитуда низкочастотных волн RR-интервала при обоих воздействиях снижалась, степень снижения не различалась между тестами и не изменялась под влиянием гравитационной разгрузки. α-коэффициент (отношение амплитуды низкочастотных волн RR-интервала и систолического АД) одинаково уменьшался в двух тестах до гравитационной разгрузки, однако после нее степень снижения α-коэффициента увеличивалась при ОТ, но не изменялась при ОДНТ. Таким образом, влияние гравитационной разгрузки на чувствительность кардиохронотропного барорефлекса проявляется при ОТ, но не при ОДНТ, что может объясняться более выраженным влиянием ОТ на механизмы нервной регуляции ритма сердца.

baroreflexgravitational unloadingsystolic blood pressureRR-interval durationα-coefficientбарорефлексгравитационная разгрузкасистолическое артериальное давлениедлительность RR-интервалаα-коэффициентИнститут медико-биологических проблем РАН (тема)Institute of Medical and Biological Problems of the Russian Academy of Sciences (topic)64.1Российский фонд фундаментальных исследований, грант (проект)Russian Foundation for Basic Research, grant (project)20-015-00536Julien C (2020) An update on the enigma of Mayer waves. Cardiovasc Res 116: E210–E211. https://doi.org/10.1093/CVR/CVZ327Julien C (2006) The enigma of Mayer waves: Facts and models. Cardiovasc Res 70: 12–21. https://doi.org/10.1016/j.cardiores.2005.11.008Tanaka K, Nishimura N, Sato M, Kanikowska D, Shimizu Y, Inukai Y, Abe C, Iwata C, Morita H, Iwase S, Sugenoya J (2013) Arterial pressure oscillation and muscle sympathetic nerve activity after 20days of head-down bed rest. Auton Neurosci Basic Clin 177: 266–270. https://doi.org/10.1016/j.autneu.2013.02.025Furlan R, Porta A, Costa F, Tank J, Baker L, Schiavi R, Robertson D, Malliani A, Mosqueda-Garcia R (2000) Oscillatory patterns in sympathetic neural discharge and cardiovascular variables during orthostatic stimulus. Circulation 101: 886–892. https://doi.org/10.1161/01.CIR.101.8.886Elghozi J-L, Julien C (2007) Sympathetic control of short-term heart rate variability and its pharmacological modulation. Fundam Clin Pharmacol 21: 337–347. https://doi.org/10.1111/j.1472-8206.2007.00502.xde Abreu S, Amirova L, Murphy R, Wallace R, Twomey L, Gauquelin-Koch G, Raverot V, Larcher F, Custaud MA, Navasiolava N (2017) Multi-system deconditioning in 3-day dry immersion without daily raise. Front Physiol 8. https://doi.org/10.3389/fphys.2017.00799Baisch F, Beck L, Blomqvist G, Wolfram G, Drescher J, Rome JL, Drummer C (2000) Cardiovascular response to lower body negative pressure stimulation before, during, and after space flight. Eur J Clin Invest 30: 1055–1065. https://doi.org/10.1046/j.1365-2362.2000.00750.xPagani M, Somers V, Furlan R, Dell’Orto S, Conway J, Baselli G, Cerutti S, Sleight P, Malliani A (1988) Changes in autonomic regulation induced by physical training in mild hypertension. Hypertens (Dallas, Tex 1979) 12: 600–610. https://doi.org/10.1161/01.HYP.12.6.600Eckberg DL, Halliwill JR, Beightol LA, Brown TE, Taylor JA, Goble R (2010) Human vagal baroreflex mechanisms in space. J Physiol 588: 1129–1138. https://doi.org/10.1113/JPHYSIOL.2009.186650Fritsch-Yelle JM, Charles JB, Jones MM, Beightol LA, Eckberg DL (1994) Spaceflight alters autonomic regulation of arterial pressure in humans. J Appl Physiol 77: 1776–1783. https://doi.org/10.1152/JAPPL.1994.77.4.1776Hughson RL, Shoemaker JK, Blaber AP, Arbeille P, Greaves DK, Pereira-Junior PP, Xu D (2012) Cardiovascular regulation during long-duration spaceflights to the International Space Station. J Appl Physiol 112: 719–727. https://doi.org/10.1152/japplphysiol.01196.2011Tomilovskaya E, Shigueva T, Sayenko D, Rukavishnikov I, Kozlovskaya I (2019) Dry immersion as a ground-based model of microgravity physiological effects. Front Physiol 10. https://doi.org/10.3389/fphys.2019.00284Borovik AS, Orlova EA, Tomilovskaya ES, Tarasova OS, Vinogradova OL (2020) Phase coupling between baroreflex oscillations of blood pressure and heart rate changes in 21-day dry immersion. Front Physiol 11: 455. https://doi.org/10.3389/fphys.2020.00455Navasiolava NM, Custaud MA, Tomilovskaya ES, Larina IM, Mano T, Gauquelin-Koch G, Gharib C, Kozlovskaya IB (2011) Long-term dry immersion: Review and prospects. Eur J Appl Physiol 111: 1235–1260.Iwase S, Sugiyama Y, Miwa C, Kamiya A, Mano T, Ohira Y, Shenkman B, Egorov AI, Kozlovs- kaya IB (2000) Effects of three days of dry immersion on muscle sympathetic nerve activity and arterial blood pressure in humans. J Auton Nerv Syst 79: 156–164. https://doi.org/10.1016/s0165-1838(99)00076-4Vinogradova OL, Popov DV, Saenko IV, Kozlovskaya IB (2002) Muscle transverse stiffness and venous compliance under conditions of simulated supportlessness. In: Eur Space Agency (Special Publication) ESA SP. 65–67.Eckberg DL (2003) Bursting into space: alterations of sympathetic control by space travel. Acta Physiol Scand 177: 299–311. https://doi.org/10.1046/J.1365-201X.2003.01073.XFu Q, Shibata S, Hastings JL, Prasad A, Palmer MD, Levine BD (2009) Evidence for unloading arterial baroreceptors during low levels of lower body negative pressure in humans. Am J Physiol Hear Circ Physiol 296. https://doi.org/10.1152/ajpheart.00184.2008Goswami N, Blaber AP, Hinghofer-Szalkay H, Convertino VA (2019) Lower Body Negative Pressure: Physiological Effects, Applications, and Implementation. Physiol Rev 99: 807–851. https://doi.org/10.1152/PHYSREV.00006.2018Stewart JM (2012) Mechanisms of sympathetic regulation in orthostatic intolerance. J Appl Physiol 113: 1659–1668. https://doi.org/10.1152/japplphysiol.00266.2012Zhedyaev RY, Tarasova OS, Sharova AP, Tomilovskaya ES, Vinogradova OL, Borovik AS (2023) Diverse effects of seven-day dry immersion on hemodynamic responses in head-up tilt and lower body negative pressure tests. Acta Astronaut 208: 105–110. https://doi.org/10.1016/j.actaastro.2023.04.005Levine BD, Pawelczyk JA, Ertl AC, Cox JF, Zuckerman JH, Diedrich A, Biaggioni I, Ray CA, Smith ML, Iwase S, Saito M, Sugiyama Y, Mano T, Zhang R, Iwasaki K, Lane LD, Buckey JC, Cookeh WH, Baisch FJ, Robertson D, Eckberg DL, Blomqvist CG (2002) Human muscle sympathetic neural and haemodynamic responses to tilt following spaceflight. J Physiol 538: 331–340. https://doi.org/10.1113/JPHYSIOL.2001.012575Ertl AC, Diedrich A, Biaggioni I, Levine BD, Robertson RM, Cox JF, Zuckerman JH, Pawel- czykd JA, Ray CA, Buckey JC, Lane LD, Shiavi R, Gaffney FA, Costa F, Holt C, Blomqvist CA, Eckberg DL, Baisch FJ, Robertson D (2002) Human muscle sympathetic nerve activity and plasma noradrenaline kinetics in space. J Physiol 538: 321–329. https://doi.org/10.1113/jphysiol.2001.012576Smit AAJ, Timmers HJLM, Wieling W, Wagenaar M, Marres HAM, Lenders JWM, van Montfrans GA, Karemaker JM (2002) Long-term effects of carotid sinus denervation on arterial blood pressure in humans. Circulation 105: 1329–1335Tanaka K, Abe C, Awazu C, Morita H (2009) Vestibular system plays a significant role in arterial pressure control during head-up tilt in young subjects. Auton Neurosci 148: 90–96. https://doi.org/10.1016/J.AUTNEU.2009.03.007Harms MPM, Finucane C, Pérez-Denia L, Jurachek S, van Wijnen VK, Lipsitz LA, van Lies- hout JJ, Wieling W (2021) Systemic and cerebral circulatory adjustment within the first 60 s after active standing: An integrative physiological view. Auton Neurosci 231. https://doi.org/10.1016/J.AUTNEU.2020.102756Schwartz CE, Medow MS, Messer Z, Stewart JM (2013) Spontaneous fluctuation indices of the cardiovagal baroreflex accurately measure the baroreflex sensitivity at the operating point during upright tilt. Am J Physiol Integr Comp Physiol 304: R1107–R1113. https://doi.org/10.1152/ajpregu.00559.2012Xiang L, Hinojosa-Laborde C, Ryan KL, Rickards CA, Convertino VA (2018) Time course of compensatory physiological responses to central hypovolemia in high- and low-tolerant human subjects. Am J Physiol Regul Integr Comp Physiol 315: R408–R416. https://doi.org/10.1152/AJPREGU.00361.2017Sugawara J, Tanabe T, Miyachi M, Yamamoto K, Takahashi K, Iemitsu M, Otsuki T, Homma S, Maeda S, Ajisaka R, Matsuda M (2003) Non-invasive assessment of cardiac output during exercise in healthy young humans: Comparison between Modelflow method and Doppler echocardiography method. Acta Physiol Scand 179: 361–366. https://doi.org/10.1046/j.0001-6772.2003.01211.xKozlovskaya IB, Grigoriev AI, Stepantzov VI (1995) Countermeasure of the negative effects of weightlessness on physical systems in long-term space flights. Acta Astronaut 36: 661–668. https://doi.org/10.1016/0094-5765(95)00156-5Negulyaev VO, Orlova EA, Sharova AP, Tarasova OS, Vinogradova OL, Borovik AS (2021) Increase in the strength of synchronization between the baroreflex waves of blood pressure and heart rate due to the lower body negative pressure effect. Hum Physiol 47: 398–403. https://doi.org/10.1134/S0362119721040125Lilly JM, Olhede SC (2012) Generalized Morse Wavelets as a Superfamily of Analytic Wavelets. IEEE Trans Signal Process 60: 6036–6041. https://doi.org/10.1109/TSP.2012.2210890Buckey JC, Lane LD, Levine BD, Watenpaugh DE, Wright SJ, Moore WE, Gaffney FA, Blomqvist CG (1996) Orthostatic intolerance after spaceflight. J Appl Physiol 81: 7–18. https://doi.org/10.1152/JAPPL.1996.81.1.7Herault S, Fomina G, Alferova I, Kotovskaya A, Poliakov V, Arbeille P (2000) Cardiac, arterial and venous adaptation to weightlessness during 6-month MIR spaceflights with and without thigh cuffs (bracelets). Eur J Appl Physiol 81: 384–390. https://doi.org/10.1007/s004210050058Pump B, Gabrielsen A, Christensen NJ, Bie P, Bestle M, Norsk P (1999) Mechanisms of inhibition of vasopressin release during moderate antiorthostatic posture change in humans. Am J Physiol Regul Integr Comp Physiol 277: 229–235. https://doi.org/10.1152/ajpregu.1999.277.1.r229Barbic F, Heusser K, Minonzio M, Shiffer D, Cairo B, Tank J, Jordan J, Diedrich A, Gauger P, Zamuner RA, Porta A, Furlan R (2019) Effects of prolonged head-down bed rest on cardiac and vascular baroreceptor modulation and orthostatic tolerance in healthy individuals. Front Physiol 10: 1–9. https://doi.org/10.3389/fphys.2019.01061Taylor JA, Eckberg DL (1996) Fundamental relations between short-term RR interval and arterial pressure oscillations in humans. Circulation 93: 1527–1532.Camm A, Malik M, Bigger J (1996) Heart rate variability. Standards of measurement, physiological interpretation, and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Eur Heart J 17: 354–381.Yokobori Y, Nakane H, Uehara C, Nagasawa T, Mitsuyama S, Ohkawa K, Kario K, Ozawa S (2023) Temporal relationships among changes in the RR-interval and the powers of the low- and high-frequency components of heart rate variability in normal subjects. Physiol Rep 11. https://doi.org/10.14814/PHY2.15557Clemson PT, Hoag JB, Cooke WH, Eckberg DL, Stefanovska A (2022) Beyond the baroreflex: a new measure of autonomic regulation based on the time-frequency assessment of variability, phase coherence and couplings. Front Netw Physiol 2. https://doi.org/10.3389/FNETP.2022.891604Ogoh S, Yoshiga CC, Secher NH, Raven PB (2006) Carotid-cardiac baroreflex function does not influence blood pressure regulation during head-up tilt in humans. J Physiol Sci 56: 227–233. https://doi.org/10.2170/physiolsci.RP001306Akimoto T, Sugawara J, Ichikawa D, Terada N, Fadel PJ, Ogoh S (2011) Enhanced open-loop but not closed-loop cardiac baroreflex sensitivity during orthostatic stress in humans. Am J Physiol Integr Comp Physiol 301: R1591–R1598. https://doi.org/10.1152/ajpregu.00347.2011