ISSN 00063509, Biophysics, 2014, Vol. 59, No. 6, pp. 965–972. © Pleiades Publishing, Inc., 2014. Original Russian Text © T.A. Zenchenko, M. Jordanova, L.V. Poskotinova, A.A. Medvedeva, A.E. Alenikova, N.I. Khorseva, 2014, published in Biofizika, 2014, Vol. 59, No. 6, pp. 1186–1194.
COMPLEX SYSTEMS BIOPHYSICS
Synchronization between Human Heart Rate Dynamics and Pc5 Geomagnetic Pulsations at Different Latitudes T. A. Zenchenkoa, b, M. Jordanovac, L. V. Poskotinovad, A. A. Medvedevaa, A. E. Alenikovad, and N. I. Khorsevab a Institute
of Theoretical and Experimental Biophysics, Russian Academy of Sciences, Pushchino, Moscow oblast, 142290 Russia b Space Research Institute, Russian Academy of Sciences, Moscow, 117997 Russia c Space Research and Technology Institute, Bulgarian Academy of Sciences, Sofia, 1113 Bulgaria d Institute of Environmental Physiology, Ural Branch, Russian Academy of Sciences, Arkhangelsk, 163000 Russia email:
[email protected] Received February 10, 2014; in final form, June 2, 2014
Abstract—Eight experiments on synchronized monitoring of cardiac indices at rest in six healthy women were conducted simultaneously at three geographical locations: Sofia, Moscow, and Arkhangelsk. By com paring the spectra of dynamic time series of the subjects' pulse and of variations in the horizontal component of the geomagnetic field vector in the frequency range of Pc5 geomagnetic pulsations, it was shown that the main oscillation periods represented in the physiological and geophysical time series largely coincide. This effect was pronounced to approximately the same extent in volunteers who participated in the experiment at all three geographic locations. Keywords: solar–biosphere connection, synchronization of rhythms, geomagnetic field variations, Pc5 geo magnetic pulsations, heart rate variations DOI: 10.1134/S0006350914060256
INTRODUCTION Since the 1970s, it has been repeatedly noticed that characteristic spectral frequencies of geomagnetic oscillations are often similar to those of major physio logical processes in living organisms (see, for example, [1–11]). The experimental evidence that has begun to be gathered in the last decade suggests that this is not a simple similarity of frequency ranges but rather a dynamical association between physiological pro cesses in the human organism and oscillations of the geomagnetic field (GMF) vector. It was shown that the intensity of brain processes was correlated with the amplitude of the principal Schumann resonance mode (8 Hz) [6, 11], while heart rate fluctuations in healthy subjects were associated with the dominant mode fre quency of the background electromagnetic field in the frequency range of 0.8–2.5 Hz [4, 5]. It should be noted that fluctuations in physiological processes, including those affecting the current heart rate, are characterized with frequencies of a much wider range than those analyzed in the studies cited above. For instance, circumstantial evidence suggests that hor mone synthesis can exhibit a periodical dynamics with periods of up to dozens of minutes [12]. A recent study that we carried out showed experimentally that station Abbreviations: GMF—geomagnetic field.
ary periods of the same range characterize the variations of such biochemical parameters as blood levels of corti sol, triiodothyronine, glucose, or nitric oxide [13]. It was also hypothesized that GMF can affect human physiology by modulating the secretion rates of impor tant hormones, such as melatonin [7, 8]. In the geomagnetic field, this frequency range cor responds to pulsations continuous, Pc5 (150–600 s) and Pc6 (>600 s). These pulsations are nearly con stantly present in the magnetosphere and, in contrast to other types of geomagnetic pulsations, are charac terized with considerable amplitudes, reaching 30– 100 nT in auroral latitudes and up to 300–600 nT dur ing strong geomagnetic perturbations [14]. For instance, the initial phase of a geomagnetic storm occurring when the turbulent front of a magnetic cloud approaches the Earth’s orbit is known to induce longperiodical Pc5/Pc6 geomagnetic pulsations with a period of 5–20 min [15]. It is now generally accepted that the classical morning and daytime Pc5 pulsations of the magnetosphere are toroidal Alfven resonance oscillations of GMF lines of force [16, 17]. Their period depends on the length of the line of force; i.e., it increases with growing latitude. We have previously shown that the spectra of varia tions in the heart rates in healthy people and in the components of the GMF vector in the Pc5–Pc6 fre
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quency range contain similar periods, which, more over, occur at approximately the same moments of time. This phenomenon was observed in 60% of exper iments performed in a single volunteer in Moscow (Russia) and in a group of 30 healthy volunteers [18]. Thus, synchronization was detected fairly frequently, but not always, both in a single person and in a group of subjects. It is still, however, unknown what condi tions are required for the phenomenon to be observed. At the same time, it is known that the amplitude of variations of the GMF vector diminishes with decreas ing latitude. The purpose of this study was to evaluate the possibility to observe the above phenomenon depending on the latitude of the observation site. For this purpose, the heart rates in healthy volunteers were monitored simultaneously at three geographical loca tions: Arkhangelsk (Russia), Moscow (Russia), and Sofia (Bulgaria). EXPERIMENTAL Eight experiments on synchronized monitoring of cardiac indices at rest were performed in six healthy women aged from 27 to 55 years. Experiments were performed synchronously at the same time (07 UT, universal time) at three geographical locations: Arkhangelsk, Moscow, and Sofia. Experiments nos. 1–5 (spring–summer 2013) involved five volunteers, and experiments nos. 6–8 (winter 2013) involved six volunteers, with two at each location. Electrocardiogram (ECG) signals were registered and processed using equipment and program means developed by Meditsinskie Komp’yuternye Sistemy (Russia): a KARDI2 module for ECG registration and the Ecosan2007 software package. ECG signals from four leads were registered at rest, in a lying position after a 10min adaptation. ECG records were used to calcu late mean heart rate values for each 1min period. The geophysical parameters used were 1min val ues of the horizontal component of the GMF vector based on data from the geomagnetic stations closest to each experimental site. In particular, the closest to Arkhangelsk (64°34′ N, 40°32′ E) were the stations of Sodankyla (SOD, 67°24′ N, 26°36′ E) and Nurmijarvi (NUR, 60°30′ N, 24°36′ E); these stations are located at approximately the same distance from Arkhangelsk, but the first one lies 3° more to the North, while the other lies 4° more to the South. The closest station to Moscow (55°45′ N, 37°36′ E) was Borok (BOX, 58°4′ N, 38°14′ E), which, however, lies rather far to the Northeast. Therefore, to evaluate the geographical variability of the variation spectra of the GMF vector components and to justify the use of these data in our study, the data from Borok were addition ally compared to the data from the Kiev station located to the Southwest (KIV, 50°42′ N, 30°18′ E) from Moscow. The data for Sofia (42°40′ N, 23°20′ E)
were obtained from the Panagjurishte station (PAG, 42°30′ N, 24°12′ E) located in immediate vicinity from the experimental site. The data were retrieved from the INTERMAGNET network (International RealTime Magnetic Observatory Network, http://ottawa.intermagnet.org/Weleom_e.php). All eight experiments were performed on days with low geomagnetic activity. For instance, in the course of measurements (07–09 UT), 3h values of the global Kp index law in the range of from 0 to 1.7, according to the data from ftp://fip.ngdc.noaa.gov/ STP/GEOMAGNETIC_DATA/INDICES/KP_AP. It was decided to compare the variations for the horizontal (X) components of the GMF vector, since their values remain close even for the stations located at considerable distances provided that the geomag netic situation is stable. In contrast to the horizontal GMF component, minute variations of the vertical (Z) component strongly depend on the underlying surface at the observation site. Therefore, since in our study the experimental sites were remote from the geophys ical stations, it would have been inappropriate to uti lize the data on the dynamics of the Z component. Methods of analysis. Computations were per formed in MATLAB R2010a using builtin functions. To remove highfrequency noises, the constant com ponent, and linear trends, the signals were bandpass filtered with the Blackman–Harris window with lower and upper cutoff frequencies equal to 0.025 and 0.95 of the Nyquist frequency, respectively. In analysis of nonstationary oscillations, which is often the case for the series of physiological parame ters, it is important to take into account not only the presence of particular periods in the signal spectrum, but also the moments when they appear or disappear. Since the series under analysis were rather short (60– 120 points), they could not have been subjected to a movingwindow time–frequency transform; there fore, we applied the more appropriate technique of wavelet transform using the Morlet function (real and complex): 2
t Ψ B ( t ) = exp ⎛ – ⎞ cos ( 5t ) . ⎝ 2⎠ To facilitate the comparison of results obtained by different methods, scale characteristics calculated using by wavelet analysis were transformed into time like characteristics similar to wave periods in spectral analysis. RESULTS Figure 1 provides an illustration of synchronous variations in the heart rate of a healthy subject at rest and in the GMF vector by showing the time series of the cardiac rate values in volunteer V3 and the varia tions of the horizontal GMF component according to the data from the Borok geomagnetic station regis BIOPHYSICS
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tered on June 11, 2013. Since our purpose was to reveal the similarity of rapid variations in the two time series, lowfrequency oscillations were removed using a band pass filter with the Blackman–Harris window with lower and upper cutoff frequencies equal to 0.1 and 0.95 of the Nyquist frequency, respectively. The results of wavelet analysis for two of the eight experiments, one from the spring and the other from the winter session, are shown in Figs. 2 and 3. Figure 2 presents the experiment performed on June 11, 2013. The left column contains wavelet images of minute variations in the horizontal component of the GMF vector in the order of decreasing latitude of the site. The right column contains wavelet images of heart rate time series in volunteers located on the same latitude: rows 1 and 2, volunteers V1 and V2 (Arkhangelsk); rows 3 and 4, volunteers V3 and V4 (Moscow); and row 5, volunteer V5 (Sofia). For Arkhangelsk and Moscow, in Figs. 2 and 3, the left column shows wave let images of time series of the GMF component reg istered at the two stations closest to the experimental site, one of them lying on a higher, and the other, on a lower latitude. The wavelet spectra obtained for the two midlati tude stations, Borok and Kyiv, were very similar in all eight experiments: they coincided in the lengths of identified periods, as well as in the positions and largely the relative amplitudes of the extrema, as shown with different shades of gray in the chart. Thus, they can be considered as identical with the currently attainable accuracy in evaluation of similarity of wavelet spectra. The extent of similarity is evident from the correspond ing charts, BOXX and KIVX (Figs. 2 and 3). Based on these data, we can conclude that the spectrum of geo magnetic variations directly at the experimental site (Moscow) should be essentially similar. A comparison of wavelet spectra of the GMF X com ponent registered at the stations of Sodankyla and Nur mijarvi (SODX and NURX) showed that either these BIOPHYSICS
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spectra were nearly identical (as in Fig. 3), or they dif fered mainly by relative amplitudes of individual extrema (Fig. 2); the time–frequency dynamics of the detected periods was identical within the accuracy of the selected method of data presentation. In these cases, only those periods that were registered at both the Sodankyla and Nurmijarvi stations were considered as reliably present at the experimental site. Thus, in the experiments shown in Figs. 2 and 3, each wavelet image of heart rate time series of volun teers from Arkhangelsk and Moscow should be com pared to both geophysical spectra shown in the corre sponding rows of the left column. A comparison of spectral components of GMF variations on different latitudes showed that the period of 7–10 min was present, although varying in ampli tude, in all five wavelet spectra throughout the whole duration of the experiment. Similarly, it was present in all five wavelet spectra of heart rate variations. The period of 17–22 min was also present on all latitudes, but its length varied during the experiment and the dynamics differed in the North and South. At the northern stations (NURX and SODX), the beginning of the experiment was characterized with a period of approximately 17 min, split in two after min 30; one of these derived periods was gradually growing to 20–23 min by the end of observation, while the other was decreasing to 10–13 min. At mid latitudes (BOXX and KIVX), the length of this period was approximately constant and constituted 17 min, while in the South (PAGX), it was approximately 22 min in the first half of the observation period and 17 min in the second half. A comparison of this period dynamics on different latitudes with the corresponding physiological spectra showed that, in three of the five subjects (V1, V3, and V5), the wavelet spectra of cardiac indices largely reflected the latitudinal GMF characteristics described
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above. In particular, in volunteer V1, a period of approximately 17 min was observed in the beginning of the experiment, and it increased to 20–25 min in the
later part, similarly to the periods in the SODX and NURX geomagnetic spectra. In volunteer V3, this period was registered starting from minute15–20 and BIOPHYSICS
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Fig. 3. Wavelet transforms of the time series of geophysical and physiological data obtained on December 4, 2013. HR, heart rate. See Results for detailed comments. BIOPHYSICS
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Cumulative analysis of synchronization between heart rate indices and oscillations of the geomagnetic field vector in all experiments Volunteers Age, years
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remained constant until the end of the experiment, sim ilarly to the series obtained with the BOXX and KIVX data. In volunteer V5, the period was close to 22 min in the beginning of the experiment and to 17 min in its sec ond half, also in agreement with the corresponding geo physical series (PAGX). In volunteer V2, the period of 20–22 min was reg istered starting from minute 20 of the experiment and was similar in length to the period observed in the wavelet spectrum of the horizontal GMF component registered at the Sodankyla station. The 15 to 17min period observed in volunteer V4 was similar to the geophysical period characteristic of mid latitudes (BOXX and KIVX); however, in contrast to the GMF spectrum, it was observed only in the sec ond half of the experiment. Another similarity in the dynamics of physiological and geophysical time series on mid latitudes con cerned the amplitude of the 30min period, which was growing in the second half of the experiment in all four wavelet spectra (V3, V4, BOXX, KIVX). The results of an experiment representing the win ter series (December 4, 2013) are shown in Fig. 3. This experiment involved six volunteers, two at each exper imental site: rows 1 and 2, volunteers V1 and V2 (Arkhangelsk); rows 3 and 4, volunteers V4 and V6 (Moscow); and rows 5 and 6, volunteers V3 and V5 (Sofia). The wavelet spectra of variations in the hori zontal GMF component registered at Panagjurishte are shown twice (Fig. 3). The upper chart represents the wavelet image for a 120minlong series (7.00– 9.00 UT), and in the lower chart the series is 90 min long (7.00–8.30 UT), since on this day ECG was reg istered for 120 min in volunteer 3, but, for technical reasons, the data for V5 were being registered for 90 min. Therefore, in the case of low latitudes, in con trast to the other charts, only the spectra in the same row should be compared to each other.
In this experiment, the dynamics of the GMF vec tor in high and lower latitudes was characterized with the presence of a 10 to 13minlong period. A similar period was observed in the heart rates of four volun teers: V1 and V2 in the North and V3 and V5 in the South. It seems worth noting a similarity between the dynamical wavelet spectra of heart rates in Northern volunteers, which exhibited a clearly pronounced 10 to 13min period, and less clear oscillations of approximately 25 min in the second half of the exper iment. The wavelet images of heart rate time series obtained in Southern volunteers were also alike: in addition to the 13 to 15min period, they contained slower oscillations with a period that increased from 20 to over 30 min in the course of observation. On mid latitudes, time series of both geophysical (BOXX and KIVX) and physiological (V4 and V6) parameters contained a shorter period of approxi mately 10 min. The dynamics of the 22min period observed for the horizontal GMF component (BOXX and KIVX) was in good agreement with a similar period in the V4 heart rate series. However, the cardiac rate series of volunteer V6 was characterized with a period of 17, and not of 22 min; so, for this participant, the degree of synchronization was very low. The described observations are summarized in the table, where three asterisks designate the cases in which the lengths of all periods observed, as well as their dynamics (the moments of appearance and dis appearance or the changes in the average length), coincided between the geophysical and physiological spectra. Two asterisks indicate the cases in which some of the periods were not present in the geophysical and the physiological series simultaneously (provided that the other periods coincided), or where these periods were observed at different moments of time. Cases in which only one of the periods coincided between the two series are designated with a single asterisk. There were no cases of complete disagreement between the BIOPHYSICS
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series. Dashes indicate that a certain volunteer did not participate in the experiment on a particular day. The bottom row of the table shows the socalled day mean index, i.e., the total number of asterisks divided by the number of volunteers who participated in the experiment on that day. The last column shows the volunteer index, which was calculated in a similar manner. Obviously, these indices provide a very rough estimate, but still they demonstrate that Figs. 2 and 3 show typical results, neither the best nor the worst. At the same time, even the rough ranking enables a preliminary comparison of the results obtained for vol unteers on different latitudes. In particular, it shows that the volunteers characterized with the highest indi ces were from all three locations: V1 with 2.5, V3 with 2.8, and V5 with 2.6. If we disregard the results obtained for V6, who has so far participated in only three experiments, it can be noted that the index val ues were lower in the younger participants than in middleaged subjects: 2.1 in V2 (27 years) and 1.9 for V4 (32 years). All these preliminary observations must be verified in a larger experimental series. CONCLUSIONS The described experiments demonstrated that syn chronization between heart rate variations and varia tions of the horizontal component of the GMF vector can be observed not only at high, but also at middle and low, latitudes. The body of data presented in this work is insufficient to draw a conclusion as to whether the occurrence and the intensity of this effect depend on the latitude of the observation site or on the sub ject’s age. A widerscale study would be required to reach such conclusions. It is known that resonance oscillations of Pc5 geo magnetic pulsations are commonly registered on steady discrete frequencies: 1.3 mHz (12.8 min), 1.9 mHz (8.7 min), 2.6 mHz (6.4 min), and 3.4 mHz (4.9 min) (e.g., [19, 20]). It should be noted that the first two of these values are close to the periods observed in heart rate variations (Figs. 2 and 3). Certainly, the described observations can be con sidered only as pilot experiments for a larger study. However, the results already obtained justify such set ting of the problem. For instance, it remains an open question whether the geomagnetic field affects the physiological parameters directly or whether there is a need to search for some further synchronized environ mental factor, e.g., variations in the atmospheric elec tric field. It has been repeatedly reported that different processes are characterized with similar sets of oscilla tion periods [13, 21, 22]. Certainly, a comprehensive investigation of the described phenomenon will, first of all, require an adequate formalism to enable quantitative evaluation of similarities between the dynamics of geophysical and physiological time series taking into account the BIOPHYSICS
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nonstationary nature of the periods in question. In addition, the selected criterion will have to be cali brated to determine the threshold values correspond ing to high, moderate, and low levels of similarity. To accomplish these tasks, a substantial longterm effort will be required, including accumulation of a consid erably larger body of experimental data. This work has already been started by our research group. This study addresses issues that are important not only for fundamental biophysics, but also for medical practice. A pilot study was performed in healthy indi viduals whose organisms possessed substantial adap tive resources, and GMF variations did not bring them beyond the limits of the physiological norm. However, in individuals suffering from certain cardiovascular disorders, such as sinus node dysfunction, the external influence affecting the generation of the cardiac impulse may constitute a risk factor. Such external fac tors can increase the risk of pacemaker wandering; premature heart beats, especially polytopic; paroxys mal tachycardia; and other conditions that might seri ously affect the myocardial contractile function. In patients with a long history of cardiac diseases, e.g., arterial hypertension, ischaemic heart disease, or car diac failure, significant variations of the GMF vector can trigger such lifethreatening conditions as cardiac fibrillation or atrial or ventricular flutter. From the point of view of biophysics, the described phenomenon of synchronization between the heart rate variations in a healthy person and oscillations of the GMF vector may provide an efficient approach to one of the central problems of geobiophysics, that is, identification of specific physiological mechanisms that underlie the biosystems' reaction to lowampli tude variations in environmental factors. ACKNOWLEDGMENTS The results presented in this article were obtained using geophysical data collected at the Sodankyla, Nur mijarvi, Borok, Kyiv, and Panagjurishte observatories. We are grateful to the staff of the Sodankylan Geofysiikan Observatorio, the Finnish Meteorologi cal Institute, the Borok Geophysical Observatory, the Institute of Geophysics of the National Academy of Sciences of Ukraine, and the Geophysical Institute of the Bulgarian Academy of Sciences for the data pro vided and for their activity in the INTERMAGNET project aimed at the promoting high standards of geo physical observations (www.intermagnet.org). REFERENCES 1. B. M. Vladimirskii and A. M. Volynskii, in Responses of Biological Systems to Weak Electromagnetic Fields (Moscow, 1971) [in Russian]. 2. B. M. Vladimirskii, N. A. Temur’yants, Effects of Solar Activity on the Biosphere–Noosphere, Ed. by L.A. Bly
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