Electromyographic Characteristics of Women in Different Phases of the Menstrual Cycle, Depending on Season and Type of Autonomic Regulation. A. Yu.
ISSN 03621197, Human Physiology, 2014, Vol. 40, No. 1, pp. 97–104. © Pleiades Publishing, Inc., 2014. Original Russian Text © A.Yu. Meigal, N.V. Voronova, L.E. Yelaeva, G.I. Kuz’mina, 2014, published in Fiziologiya Cheloveka, 2014, Vol. 40, No. 1, pp. 113–121.
Electromyographic Characteristics of Women in Different Phases of the Menstrual Cycle, Depending on Season and Type of Autonomic Regulation A. Yu. Meigal, N. V. Voronova, L. E. Yelaeva, and G. I. Kuz’mina Petrozavodsk State University, Petrozavodsk, 185640 Karelia, Russia Received October 9, 2012
Abstract—Quantitative characteristics of the neuromuscular state in women (n = 23; age, 19.9 ± 1.4 years) were studied in four (early and late follicular, ovulatory, and luteal) phases of the menstrual cycle, in the spring and autumn/winter seasons, depending on the type of regulation of the autonomic nervous system, based on linear and novel nonlinear parameters of interference electromyography in m. biceps br. and the activity of the motor units of m. triceps br. Statistically significant differences in the neuromuscular state, such as a decrease in all nonlinear parameters, i.e., simplification of the temporal structure of the interference elec tromyography signal and an increase in the frequency of impulses of motor units, are due to the combined effect of the ovulatory phase and the spring season. In addition, the greatest influences on the neuromuscular state were recorded in subjects with the vagotonic type of regulation of the autonomic nervous system. Keywords: menstrual cycle, electromyography, neuromuscular state, nonlinear parameters, motor units, cli matic–geographic conditions DOI: 10.1134/S0362119714010113
Skeletal muscles are highly adaptable to longact ing environmental factors, such as temperature, oxy genation, and microgravity, as well as to physical states, such as immobilization, aging, exercise, and atrophy [1]. Menstrual cycle (MC) with the related cyclic changes in the levels of sex hormones is a spe cific state of the female body that affects other func tions, such as the state of the skeletal muscles, auto nomic state, and thermoregulation. The functioning of skeletal muscles in women during different phases of the MC constantly attracts interest. It is believed that the menstrual phase can affect the achievement of a good athletic shape for competition, strength, endurance, risk of injury, fatigue, coordination, and metabolism [2–4]. Cyclic changes in the ratio of estrogen, progesterone, testosterone, and gonadotro pic hormone affect the state of the central nervous sys tem (CNS) [5], which, in turn, affects emotional and motivational spheres of women [6, 7]. In general, progesterone and estrogens cause oppo site effects on the excitability of the neural tissue. Estrogens increase the excitability of the CNS, while progesterone decreases it, which may be due to the influence of hormones and their derivatives in the brain (neurosteroids) on the current levels of GABA, glutamate, dopamine, and serotonergic mecha nisms [5, 8]. There are sexrelated differences in mus cle contraction. Several studies have shown that women are more resistant to fatigue [9, 10]. The mechanism of these differences becomes clear from
the experimental studies in animals, which show that the removal of estrogen (ovariectomy) leads to the transformation of the intermediate muscle fibers (IIA) to faster muscle fibers (IIB) [11]. Similarly, in male rats, castration leads to an increase in the proportion of the muscle fibers of IIA type (intermediate), and androgenization leads to an increase in the proportion of fast muscle fibers of IIB type [12]. However, the data on the effect of varying concentrations of sex hor mones, i.e., the menstrual phase, on the state of the motor system and achievement of good athletic shape are still contradictory. In most studies on the effect of the MC on women’s body functions, primarily, the follicular and luteal phases are studied, because they are clearly different in many ways [13]. Early or late follicular phases, early or late luteal phases, the menstruation period, the pre menstrual period, and ovulatory phase are studied in a number of works. Usually, no more than two or three different phases of the MC are considered in one study, and the results are difficult to compare. In this context, we supposed it interesting to study four phases of MC, which most clearly differ in the levels of sex hormones: an early follicular (low levels of sex hor mones), late follicular (rising levels of estrogen, low progesterone), ovulatory (high testosterone), and luteal (high progesterone and estrogen levels) phases. Seasonality (the annual cycle) plays an important role in the human life. Many body functions, includ ing the female reproductive function, vary during the 97
98
MEIGAL et al.
annual cycle [14, 15]. In this context, we considered it crucial to evaluate the neuromuscular state (NMS) of women not only in different phases of the MC, but in two different seasons (spring and autumn), taking into account the type of autonomic regulation (vagotonic, normotonic, or sympathotonic) [16]. The interference electromyogram (iEMG) and the parameters of activity of motor units (MUs) provide the assessment of the NMS (motor strategies) in humans [17, 18]; therefore, they are often used in studies on the motor system. The use of novel nonlin ear parameters of biological signals, such as the corre lation dimension and entropy, for assessing NMS showed their greater value, compared to linear param eters, in the diagnosis of Parkinson’s disease [19, 20] and also in comparing iEMGs in men and women [21]. It was recently shown [22] that the phase of MC does not affect the linear parameters of the surface EMG, except the nerve conduction velocity and the degree of the decrease in the iEMG rate during fatigue. In the literature, there are no data on the dynamics of nonlinear parameters of iEMG during the MC. Nor are there data on the activity of MUs during different phases of MC. Therefore, the goal of this study was to estimate how the season (autumn/winter or spring), the type of autonomic regulation, and the menstrual phase affect the neuromuscular state of women based on the cuta neous electromyography with traditional linear and novel nonlinear parameters of iEMG and the activity of motor units. EXPERIMENTAL The dynamics of the parameters of iEMG and MUs was studies for a year, during two seasons: autumn/winter season (from October to January) and spring (from March to May), in women during four phases of the MC, depending on the type of regulation of the autonomic nervous system. The study was con ducted in 2009–2011. In total, the study involved 29 healthy women aged 18 to 24 years (mean age, 19.9 ± 1.4 years), nonsmok ers, who did not use hormonal contraception. The experiment was conducted on the grounds of their written informed consent and the permission of the Ethics Committee of the Health Ministry of the Republic of Karelia. During the experiment, three subjects for various reasons cancelled their participa tion; one subject had anovulatory MC; and two sub jects had irregular MC. Thus, the results of our study are based on the data on 23 subjects. The following four phases of the MC were studied: (1) the early follicular phase (F1), on average, was studied on day 7 of the MC; (2) the late follicular phase (F2), on average, was studied on day 13 of MC; (3) the ovulatory phase (OV), on day 16 of MC; and (4) the luteal phase (LUT), on day 24 of MC. These days almost coincide with the respective days in other
studies [23]. The average length of MC throughout the study period was 28.84 ± 0.32 days (in the autumn/winter season, 28.62 ± 0.71 days; in spring, 29.16 ± 0.82 days, p > 0.05). The moment of ovulation was verified by measuring basal body temperature. All subjects kept a diary of basal body temperature. On the same day, at the same time, autonomic parameters were studied in subjects by analyzing heartbeat time series with the use of a Vegetotester (VNSSpectrum, Neurosoft, Ivanovo, Russia). Based on the data obtained, using Baeskii’s method of study ing the heart rhythm [16], all the subjects were divided into three groups: normotonics, vagotonics, and sym patotonics. All tests were performed in the first half of the day, from 10 a.m. to noon, in order to avoid the influence of diurnal variations of hormones, such as glucocorti coids. The phase of the MC and the day of ovulation were determined by measuring the basal body temperature (BT) and plotting BT. After detailed instructions, each subject performed measurements and plotted the BT individually. The measurements were carried out rec tally, for 30 s, with an electronic thermometer (DT 520, A&D, Tokyo, Japan), which was used individu ally throughout the study. An infrared thermometer was not used because we consider it inaccurate due to the nature of the contact of the measuring nozzle and the skin at the muscle of the anus. The duration of uninterrupted sleep before measuring the BT was at least 6 h. The thermometer was located in the imme diate vicinity of the bed, so that the subjects had no need to get up and stretch out for it. Measurements of BT were performed daily, with no breaks for menstru ation, illness, holidays, etc., for at least three men strual cycles prior to the study and throughout the study period. The measurements were made at the same time of the day: the time difference should not exceed 30 min. In the morning, after waking up, with out getting out of bed, or sitting down, or making sud den movements, the subjects carefully put the narrow part of the thermometer into the rectum. The surface iEMG was recorded from the m. biceps br. of the dominant side (usually, the right side, 91.3%), in the standing position, with the shoul der dropped down along the body, and the upper arm held in a position of elbow flexion of 90°, parallel to the floor. The iEMG records were made at a load of 0 (no load), 1, 2, and 3 kg, using a NeuroMEP8 elec tromyograph (Neurosoft, Ivanovo, Russia). Record ing electrodes were attached to the hand over the mus cle by means of standard medical adhesive bandage. The skin was pretreated with abrasive paste and 70% ethanol; the electrode was applied with the electrode gel (Viasis Health Care, Surray, United Kingdom). The bandwidth of the EMG was 20–1000 Hz. EMG segments with a duration of 1 s were recorded. The NeuroMEP8 apparatus enabled us to obtain the lin ear parameters of iEMG, including the average ampli HUMAN PHYSIOLOGY
Vol. 40
No. 1
2014
ELECTROMYOGRAPHIC CHARACTERISTICS OF WOMEN IN DIFFERENT PHASE
tude (A, μV) and the average frequency (MNF, Hz). We used the FRACTAN 4.4 © software to characterize the attractor of iEMG, which is described by nonlin ear parameters, such as the fractal dimension (D), cor relation dimension (Dc), and correlation entropy (К2) [4]. More than 1000 samples of iEMG were analyzed. Electromyograms were tested for the presence of a trend. The trend was small; it was, approximately, the same in all the samples of iEMG and affected nonlin ear parameters of iEMG to a minimal extent. There fore, the FRACTAN 4.4 © software was used directly for detrending the samples of iEMG. In addition, the parameters of the series of impulses of the MUs of m. triceps br. were recorded in the dom inant and nondominant hands, i.e., bilaterally, according to the method that we used previously [23]. The subjects were asked to strain the muscle until the MUs began to impulse spontaneously and do not try to control these MUs or specifically support their impulses. Only the MUs that generated impulses sus tainably and did not require additional control were analyzed. The recording time of the activity of the MUs was 10 s. From 70 to 100 interimpulse intervals were analyzed, and the average interimpulse interval (IPI, ms), the average frequency of impulses (f, imp/s), and variability (standard deviation of the mean pulse interval, σ, ms) were calculated. Thus, for the characterization of the NMS, totally, eight elec tromyographic parameters were taken into consider ation. Statistical analysis was performed using the Stat graphics 15.0 Centurion software. The influence of the phase of MC, the season, and the type of regulation of the autonomic nervous system (ANS) on the parame ters of iEMG was determined using nonparametric tests (the Mann–Whitney and Kruskal–Wallis tests). The results were considered statistically significant at p < 0.05. RESULTS Of the 29 women who participated in the study, 23 subjects (79.3%) passed all the tests, six subjects, for various reasons, left the study. According to the results of analysis of heartbeat time series, all subjects were divided into groups of normotonics (n = 12; 52.17%), vagotonics (n = 9; 39.13%), and sympathotonics (n = 2; 8.7%). Henceforth, the comparisons were made only between the groups of normotonics and vagotonics. Activity of the Motor Units In total, the activity of 467 MUs was recorded. It was found that the average IPI for the dominant hand was 116.47 ± 19.48 ms (n = 247), and for the nondom inant hand, 121.91 ± 21.95 ms (n = 220, p > 0.05, with respect to the dominant hand). Applying only the fac tor of the phase of the MC showed that menstrual phase does not affect the average IPI or the average HUMAN PHYSIOLOGY
Vol. 40
No. 1
2014
99
Table 1. The average interimpulse interval of the motor units of dominant and nondominant hands, depending on the phase of the menstrual cycle Phase of the Dominant hand menstrual cycle F1 F2 OV LUT Total
Nondominant hand
117 ± 18 (n = 71) 123 ± 21 (n = 63) 116 ± 22 (n = 59) 121.6 ± 25 (n = 56) 115 ± 20 (n = 38) 120.789 ± 20 (n = 37) 117 ± 19 (n = 79) 121.745 ± 22 (n = 64) 116 ± 19 (n = 247) 121.91 ± 22 (n = 220)
No statistically significant differences.
Table 2. The average interimpulse interval and rate of impulsing of the motor units of dominant and nondominant hands, depending on the season Side Dominant hand Nondomi nant hand
Autumn
Spring
120 ± 19 (n = 122)** 8.6 ± 1.3** 123 ± 23 (n = 119) 8.4 ± 2.0
112 ± 22 (n = 125)## 9.1 ± 1.7## 120 ± 21 (n = 101) 8.6 ± 1.6
The top row, the average interimpulse interval (ms); the bottom row, the rate of impulsing (imp/s); ** p < 0.01 compared to spring; ## p < 0.01 compared to the nondominant hand.
frequency of the impulses of MUs (Table1). Analysis of the season factor alone, excluding the menstrual phase, showed that there is a trend towards a decrease in the IPI in the spring season, and this trend is statis tically significant for the dominant hand (Table 2). The frequency of impulses of MUs for the dominant hand in the spring was ~9 imp/s, while in autumn, it was ~8 imp/s (p < 0.05). Analysis of the seasonal factor combined with the factor of the phase of MC showed that their combined influence on the activity of MUs is more distinct. There was a statistically significant increase in the fre quency of impulses in the nondominant hand in the ovulatory phase in the spring and in the dominant hand during the luteal phase (Table 3). Further increase in the number of the factors to three, i.e., (1) season, (2) the phase of MC, and (3) the type of regulation of the ANS, did not lead to an increase in the differences in the parameters of the activity of the MUs under study. However, in the ovu latory phase, in spring, in particular, in the group of vagotonics, the frequency of impulses of MUs (in both hands) was the greatest, up to 9.5 imp/s (p > 0.05). Linear and Nonlinear Parameters of iEMG The average amplitude of the iEMG of the biceps increased monotonically with increasing the load on the elbow joint from 70–80 μV at 0 kg (unloaded) to
100
MEIGAL et al.
Table 3. The average interimpulse interval and rate of impulsing (imp/s) of the motor units of dominant and non dominant hands, depending on the phase of the menstrual cycle and the season Phase F1 F2 OV LUT
F1 F2 OV LUT
Autumn
Spring
Dominant hand 120 ± 18 (n = 33) 114 ± 17 (n = 38) 8.5 ± 1.3 8.1 ± 1.4 118 ± 19 (n = 32) 115 ± 24 (n = 27) 8.7 ± 1.3 9.1 ± 1.9 117 ± 18 (n = 18) 114 ± 23 (n = 20) 8.8 ± 1.5 9.2 ± 2.2 122 ± 20 (n = 39) 112 ± 17.6 (n = 40)*# 8.4 ± 1.4 9.2 ± 1.6*# Nondominant hand 126 ± 23 (n = 29) 121 ± 19 (n = 34) 8.14 ± 1.55 8.50 ± 1.47 121 ± 27 (n = 33) 123 ± 23 (n = 23) 8.7 ± 2.2 8.6 ± 2.0 114 ± 24 (n = 15) 125 ± 15.0 (n = 22) 8.0 ± 1.0 9.2 ± 2.2* 122 ± 24 (n = 35) 122 ± 19 (n = 29) 8.7 ± 2.5 8.4 ± 1.2 *
* p < 0.05 compared to autumn; # p < 0.05 compared to the non dominant hand.
160–170 μV at a load of 3 kg. With all loads, during all phases, in both seasons, and in both hands, the fre quency remained the same, about 110–120 Hz. There were no differences in the amplitude or frequency of the iEMG in the groups of normotonics and vagoton ics. The phase of the MC considered as a single factor had no effect on any of the nonlinear parameters of iEMG (Table 4). Consideration of the seasonal factor as a single one showed that there was a tendency of a
decrease in all nonlinear parameters (fractal and cor relation dimensions and correlation entropy) in spring (Table 4). The combined use of the factors of men strual phase and season showed that the decrease in the value of all the nonlinear parameters occurred in the ovulatory phase in spring (Table 5). Adding the third factor (the type of regulation of the autonomic nervous system) showed that a decrease in the nonlin ear parameters occurred in vagotonics, in the ovula tory phase, in the spring season (Table 6). DISCUSSION The parameters of iEMG and activity of individual MUs were studied (1) during four consecutive phases of the MC in women aged 20–23 years; (2) in autumn and spring; and (3) as dependent on the type of regu lation of the autonomic nervous system. It was found that, taken separately, the phase of the MC did not affect the parameters of the iEMG, or the activity of the MUs. The factor of the season has a slightly stron ger effect. In particular, in spring, a downward trend was recorded in the nonlinear parameters of iEMG and the average IPI of the MUs, i.e., an increase in the impulse frequency. However, the greatest changes in iEMG and the activity of MUs resulted from the com bined analysis of seasonal factors and the menstrual phase; specifically, the changes were the largest in spring in the ovulatory phase. In the ovulatory phase, there was a statistically significant decrease in the val ues of all nonlinear parameters and an increase in the impulse frequency of the MUs. The linear parameters (amplitude and frequency of iEMG) were not sensitive to the season or the phase of the MC. Our data enabled us to discuss the adaptive motor strategies during the change of seasons and phases of the MC. In general, our findings are consistent with the few electromyographic results obtained by other authors. Sung et al. [21] showed that nonlinear iEMG parameters in women were more sensitive to fatigue,
Table 4. Fractal dimension (D), correlation dimension (Dc), and correlation entropy (K2) in different phases of the men strual cycle (MC) Factor F1 F2 OV LUT Autumn Spring Irrespective of the phase and the season
D
Dc
Phase of MC (irrespective of the season) 1.744 ± 0.060 (n = 142) 4.15 ± 0.32 (n = 148) 1.748 ± 0.041 (n = 118) 4.14 ± 0.32 (n = 117) 1.749 ± 0.048 (n = 80) 4.14 ± 0.32 (n = 80) 1.746 ± 0.067 (n = 148) 4.14 ± 0.34 (n = 147) Season (irrespective of the phase of MC) 1.750 ± 0.041 (n = 241) 4.18 ± 0.31 (n = 241) 1.743 ± 0.068 (n = 252) 4.11 ± 0.35 (n = 252)** 1.745 ± 0.056 (n = 493) 4.14 ± 0.34 (n = 493)
K2 4.88 ± 2.52 (n = 148) 5.01 ± 2.56 (n = 118) 4.27 ± 1.60 (n = 80) 4.66 ± 2.22 (n = 148) 4.866 ± 2.448 (n = 241) 4.627 ± 2.180 (n = 252) 4.744 ± 2.318 (n = 493)
** p < 0.01 compared to autumn. HUMAN PHYSIOLOGY
Vol. 40
No. 1
2014
ELECTROMYOGRAPHIC CHARACTERISTICS OF WOMEN IN DIFFERENT PHASE
101
Table 5. Nonlinear parameters of subjects (n = 23), depending on the phase of the menstrual cycle and season Phase F1 F2 OV LUT F1 F2 OV LUT F1 F2 OV LUT
Autumn
Spring
Fractal dimension (D) 1.748 ± 0.041 (n = 67) 1.744 ± 0.044 (n = 62) 1.758 ± 0.037 (n = 40) 1.752 ± 0.014 (n = 72) Correlation dimension (Dc) 4.12 ± 0.33 (n = 68) 4.16 ± 0.33 (n = 61) 4.25 ± 0.30 (n = 40) 4.12 ± 0.27 (n = 71) Correlation entropy (K2) 4.97 ± 2.62 (n = 68) 5.07 ± 2.56 (n = 62) 4.45 ± 1.91 (n = 40) 4.82 ± 2.48 (n = 72)
1.741 ± 0.07347 (n = 75) 1.753 ± 0.037 (n = 56) 1.740 ± 0.055 (n = 40, P = 0.066) 1.740 ± 0.085 (n = 76) 4.11 ± 0.30 (n = 80) 4.11 ± 0.31 (n = 56) 4.03 ± 0.31 (n = 40)** 4.15 ± 0.44 (n = 76) 4.80 ± 2.24 (n = 80) 4.93 ± 2.59 (n = 56) 4.09 ± 1.21 (n = 40, P = 0.16) 4.50 ± 1.94 (n = 76)
** p < 0.01 compared to autumn.
compared to linear parameters. In addition Soares et al. [22] found hardly any difference in the amplitude of iEMG in different phases of the MC; only their exper iments with exercising until fatigue showed that symp toms of fatigue sooner appeared on iEMG at the beginning and end of the follicular phase and at the end of the luteal phase. These intervals of the MC are characterized by low levels of hormones, both estrogen and progesterone [24]. Skeletal muscles are highly adaptable to environ mental factors and the state of the body, such as hypoxia, microgravity, exercise, immobilization, atro phy, cooling, and age [25]. Under the influence of these factors, the balance of different types of muscle fibers in the muscle changes in the direction of fast or slow fibers; in addition, the thickness and strength of the fibers also change. The result of structural and functional adaptation in the skeletal muscles usually appears after a few weeks or months of exposure to the factor [26]. In this regard, we assume that a small length of the phases of the MC (approximately, two weeks) does not allow the adaptive changes to be evi dent due to the short duration of the effect. Probably, these changes would be recorded after more prolonged action of the sex hormones, e.g., during pregnancy or hormone replacement therapy. In contrast to the phases of the MC, seasonal changes, such as sunlight (in Petrozavodsk, the duration of the allnight twilight season is 52 days) and tempera ture (the duration of climatic winter is 150 days) are much longer. This time should be enough to change the NMS and the activity of MUs, and, hence, the iEMG parameters. However, the hormones can affect HUMAN PHYSIOLOGY
Vol. 40
No. 1
2014
the CNS directly and rapidly, thereby, demonstrating their neuromodulatory activity [8]. The fact that, in spring, the ovulatory phase affects the NMS of women may be due to thesynergistic cooperation of hormones acting in the ovulatory phase and hormones that are active in the spring season. It is well known that the sharp increase (gradient) of illu mination, which is observed in spring, causes an increase in plasma cortisol [27]; whereas, when the illumination is stable, there is no difference in the cor tisol levels between the summer and winter seasons. It is likely that melatonin, which is reported to decrease with increasing illumination, plays a special role in the seasonal modulation of NMS [28]. The concentration of melatonin also depends on the phase of the MC, changing unidirectionally with progesterone; i.e., the level of melatonin is increased in the luteal phase [29]. However, in our study, in the luteal phase of the MC, in contrast to the ovulatory phase, the changes in iEMG and the activity of MUs were minor. The ovu latory phase itself is characterized by low levels of female hormones, reduced levels of oxytocin, and an increase in the levels of gonadotropins and testoster one [6, 30, 31]. The concentration of testosterone is also increased in the luteal phase [32, 33]. In the ovulatory phase in spring, the MU impulse frequency increases by about 10% in the nondominant hand. It is well known that there are differences in the organization of the motor neuron pool between the dominant and nondominant hands. In particular, in the nondominant hand, the frequency and variability of the MU impulses are greater than that in the domi nant hand, which is explained by the principle that the nondominant hand needs more of an effort to main
102
MEIGAL et al.
Table 6. Nonlinear parameters of subjects (n = 23), depending on the phase of the menstrual cycle, autonomic state, and season Normotonics
Vagotonics
Phase autumn (n = 12) F1 F2 OV LUT
F1 F2 OV LUT
F1 F2 OV LUT
1.746 ± 0.045 (n = 43) 1.750 ± 0.0434 (n = 36) 1.761 ± 0.0427 (n = 24) 1.763 ± 0.037 (n = 40) 4.18 ± 0.39 (n = 44) 4.13 ± 0.32 (n = 36) 4.25 ± 0.31 (n = 24) 4.13 ± 0.27 (n = 40) 5.10 ± 2.76 (n = 44) 4.99 ± 2.58 (n = 36) 4.44 ± 2.00 (n = 24) 4.90 ± 2.59 (n = 40)
spring (n = 10) Fractal dimension 1.731 ± 0.005 (n = 40) 1.747 ± 0.0368 (n = 20) 1.746 ± 0.052 (n = 28) 1.752 ± 0.042 (n = 40) Correlation dimension 4.07 ± 0.30 (n = 40) 4.05 ± 0.22 (n = 20) 4.04 ± 0.31 (n = 28)** 4.23 ± 0.46 (n = 40) Correlation entropy 4.88 ± 2.53 (n = 40) 4.51 ± 2.13 (n = 20) 4.15 ± 1.42 (n = 28) 4.47 ± 1.92 (n = 40)
autumn (n = 9)
spring (n = 12)
1.752 ± 0.001 (n = 24) 1.735 ± 0.043 (n = 26) 1.753 ± 0.029 (n = 16) 1.739 ± 0.042 (n = 32)
1.75 ± 0.050 (n = 40) 1.756 ± 0.0376 (n = 36) 1.726 ± 0.063 (n = 12) 1.728 ± 0.058 (n = 36)
4.24 ± 0.20 (n = 24)# 4.22 ± 0.35 (n = 26) 4.25 ± 0.28 (n = 16) 4.11 ± 0.28 (n = 32)
4.15 ± 0.31 (n = 40) 4.14 ± 0.35 (n = 36) 4.00 ± 0.33 (n = 12)* 4.06 ± 0.41 (n = 36)
4.74 ± 2.37 (n = 24) 5.19 ± 2.56 (n = 26) 4.46 ± 1.84 (n = 16) 4.72 ± 2.37 (n = 32)
4.71 ± 2.36 (n = 40) 5.17 ± 2.80 (n = 36) 3.95 ± 0.52 (n = 12) 4.54 ± 2.00 (n = 36)
* p < 0.09, spring vs. autumn; ** p < 0.01, spring vs. autumn; # p < 0.05 compared to the luteal phase.
tain the same contraction as the dominant hand [34]. In our study, the frequency of impulses, on the con trary, tended to be lower in the nondominant hand. Probably, this is due to our studying only spontane ously active MUs, which did not need voluntary acti vation. There is also a difference between men and women in the percentage of slow and fast muscle fibers: in women, generally, the percentage of slow fibers is 5–6% greater than in men [35]. Probably, the changes in the activity of MUs characteristic of the ovulatory phase are due to testosterone. A decrease in the nonlinear parameters of iEMG during the ovulatory phase of MC in spring indicates a clear simplification of iEMG [17, 21]. Simplification, in terms of the nonlinear dynamics of a signal, indi cates a decrease in the complexity, as well as an increase in the predictability and regularity of the sig nal. This, in turn, indicates the existence of repetitive
fragments of iEMG that are often visually indistin guishable. From the viewpoint of neurophysiology, this reflects an increase in the synchronization of the activity of MUs [36] and an increased clustering factor of the generator of a signal (in our case, the motoneu rons pool) [37]. With increased clustering, the ele ments of the generator of a signal perform integrally, which leads to the appearance of ordered repetitive fragments, resembling a tremor, in their performance. Earlier, we showed the possibility of increased deter minism of the tremor signal (accelerogram) with no visible changes in the iEMG, as exemplified by patients with Parkinson’s disease [19, 20]. We assume that the combination of two hormonal factors, test osterone and cortisol, causes a tendency of iEMG towards clustering and a trend of the activity of MUs towards synchronization found in our study. Nonlin ear parameters may characterize the functionality of HUMAN PHYSIOLOGY
Vol. 40
No. 1
2014
ELECTROMYOGRAPHIC CHARACTERISTICS OF WOMEN IN DIFFERENT PHASE
the system, i.e., the number of functions that are inherent to the system (the fractal dimension), or the number of equations that describe the behavior of the system (correlation dimension). In particular, a decrease in the fractal dimension indicates a decrease in the influence of other levels (probably, higher levels) of regulation of the motor system [38]. Since a tremor with a distinct psychogenic (emo tiogenic) component often increases in response to excitement and is decreased by βadrenergic blocking agents, we attempted to find out a sympathetic com ponent in the formation of the parameters of iEMG. In this regard, according to Baevskii’s method of recording heartbeat time series, we divided all subjects into two groups, vagotonics and normotonics, which were similar in size [16]. It was found that the type of regulation of the ANS affects the parameters of iEMG. In particular, during the ovulatory phase, in the spring season, the values of nonlinear parameters of iEMG in vagotonics were less than that in normo tonics. Despite the large amount of studies on the regula tion of the cardiovascular system during the MC, the data on blood pressure, heart rate, and the ratio of the activities of the sympathetic and parasympathetic sys tems are still controversial. Most authors report an increased activity of the sympathetic nervous system in the luteal phase [39–42]; in other studies, it is reported about this activity during menstruation or in the follicular phase [43]. There are substantially less studies on the ovulatory phase, however, it is known to be characterized by a higher systolic blood pressure [44] and high absolute values of the heart rate. Gona dotropic hormones have almost no effect on the ratio of sympathetic and parasympathetic activitieas, as can be seen from the parameters of the analysis of heart beat time series during the MC [24]. Probably, this is why the changes in the NMS were specific to the group of vagotonics, because its effect can become distinct against the background of initially reduced sympa thetic control. CONCLUSIONS Our study has shown that, during the year, the NMS of women is subjected to a statistically signifi cant combined effect of the ovulatory phase of men strual cycle and the spring season. This leads to an increase in the frequency of the impulses of motor units and the appearance of the signs of clustering (simplification) of iEMG, which is similar to the changes resulting from the effects of testosterone and the sympathetic nervous system. Indeed, androgeni zation of the body leads to the changes in the proper ties of muscle fibers towards those of fasttype fibers [12]. Probably, the biological sense of this adaptive motor strategy consists in the timely virilization of the female body for the implementation of the reproduc tive function. HUMAN PHYSIOLOGY
Vol. 40
No. 1
2014
103
ACKNOWLEDGMENTS This study was supported by the Program of Strate gic Development of Petrozavodsk State University. REFERENCES 1. Matsakas, A. and Patel, K., Skeletal muscle fibre plas ticity in response to selected environmental and physi ological stimuli, Histol. Histopathol., 2009, vol. 24, p. 611. 2. McEwen, B.S. and Alves, S.E., Estrogen actions in the central nervous system, Endocr. Rev., 1999, vol. 20, p. 279. 3. Oosthuyse, T. and Bosch, A.N., The effect of the men strual cycle on exercise metabolism: implications for exercise performance in eumenorrhoeic women, Sports Med., 2010, vol. 40, p. 207. 4. Vaiksaar, S., Jürimäe, J., Mäestu, J., Purge, P., et al., No effect of menstrual cycle phase and oral contracep tive use on endurance performance in rowers, J. Strength. Cond. Res., 2011, vol. 25, p. 1571. 5. Smith, M.J., Adams, L.F., Schmidt, P.J., Rubinow, D.R., Wassermann, E.M., et al., Abnormal luteal phase excit ability of the motor cortex in women with premenstrual syndrome, Biol. Psychiatry, 2003, vol. 54, p. 757. 6. Saunders, K.E. and Hawton, K., Suicidal behaviour and the menstrual cycle, Psychol. Med., 2006, vol. 36, p. 901. 7. BacaGarcía, E., DíazSastre, C., de Leon, J., and SaizRuiz, J., The relationship between menstrual cycle phases and suicide attempts, Psychosom. Med., 2000, vol. 62, p. 50. 8. Fedotova, Yu.O. and Sapronov, N.S., Estrogen actions in the central nervous system, Usp. Fiziol. Nauk, 2007, vol. 38, no. 2, p. 46. 9. Hicks, A.L., KentBraun, J., and Ditor, D.S., Sex dif ferences in human skeletal muscle fatigue, Exerc. Sport Sci. Rev., 2001, vol. 29, p. 109. 10. Larivière, C., Gravel, D., Gagnon, D., Gardiner, P., et al., Gender influence on fatigability of back muscles during intermittent isometric contractions: a study of neuromuscular activation patterns, Clin. Biomech., 2006, vol. 21, p. 893. 11. Liu, Y.H., Jia, S.S., and Hou, Y.X., Effects of ovariec tomy on rat genioglossal muscle contractile properties and fibertype distribution, Angle. Orthod., 2009, vol. 79, p. 509. 12. Son’kin, V.D. and Tambovtseva, R.V., Razvitie myshechnoi energetiki i rabotosposobnosti v ontogeneze (Development of muscular energetics and performance in the ontogenesis), Moscow: URSS, 2011. 13. Blondin, D.P., Maneshi, A., Imbeault, M.A., and Haman, F., Effects of the menstrual cycle on muscle recruitment and oxidative fuel selection during cold exposure, J. Appl. Physiol., 2011, vol. 111, p. 1014. 14. Poskotinova, L.V., Vegetativnaya regulyatsiya ritma ser dtsa i endokrinnyi status molodezhi v usloviyakh Evropeiskogo Severa Rossii, (Vegetative Regulation of the Cardiac Rhythm and the Endocrine State in Young Men of the European North of Russia), Yekaterinburg: UrO RAN, 2010.
104
MEIGAL et al.
15. Sezonnaya dinamika fiziologicheskikh funktsii u che loveka (Seasonal Dynamics of Physiological Functions in Humans), Boiko, E.R, Ed., Yekaterinburg: UrO RAN, 2009. 16. Baevskii, R.M., The problem of evaluation and prog nosis of the functional state of the body and its develop ment in space medicine, Usp. Fiziol. Nauk, 2006, vol. 37, no. 3, p. 42. 17. Farina, D., Merletti, R., and Enoka, R.M., The extrac tion of neural strategies from the surface EMG, J. Appl. Physiol., 2004, vol. 96, p. 1486. 18. Farina, D., Fosci, M., and Merletti, R., Motor unit recruitment strategies investigated by surface EMG variables, J. Appl. Physiol., 2002, vol. 92, no. 1, p. 235. 19. Meigal, A.Y., Rissanen, S.M., Kankaanpää, M., et al., Novel parameters of surface EMG in patients with Par kinson’s disease and healthy young and old controls, J. Electromyogr. Kinesiol, 2009, vol. 19, p. 206. 20. Meigal, A.Y., Rissanen, S.M., Tarvainen, M.P., et al., Linear and nonlinear tremor acceleration characteris tics in patients with Parkinson’s disease, Physiol. Meas., 2012, vol. 33, p. 395. 21. Sung, P.S., Zurcher, U., and Kaufman, M., Gender differences in spectral and entropic measures of erector spinae muscle fatigue, J. Rehabil. Res. Dev., 2008, vol. 45, p. 1431. 22. Soares, F.A., Salomoni, S.E., Veneziano, W.H., de Car valho, J.L., et al., On the behavior of surface elec tromyographic variables during the menstrual cycle, Physiol. Meas., 2011, vol. 32, p. 543. 23. Meigal, A.Yu., Kuz’mina, G.I., Shigueva, T.A., and Zakirova, A.Z., A method of selective derivation of the action potentials of human motor units through surface electrodes, Human Physiol., 2009, vol. 35, no. 5, p. 642. 24. Leicht, A.S., Hirning, D.A., and Allen, G.D., Heart rate variability and endogenous sex hormones during the menstrual cycle in young women, Exp. Physiol., 2003, vol. 88, p. 441. 25. Pette, D., The adaptive potential of skeletal muscle fibers, Can. J. Appl. Physiol., 2002, vol. 27, p. 423. 26. D’Antona, G., Pellegrino, M.A., Adami, R., Rossi, R., et al., The effect of ageing and immobilization on struc ture and function of human skeletal muscle fibres, J. Physiol., 2003, vol. 52, p. 499. 27. Boiko, E.R. and Tkachev, A.V., The effect of the dura tion of daylight on human hormonal and biochemical indices in the north, Fiziol. zhurn. im. I.M. Sechenova, Moscow: Sechenova, 1995, vol. 81, issue 7, p. 86. 28. Pääkkönen, T., Leppäluoto, J., Mäkinen, T.M., Rin tamäki, H., et al., Seasonal levels of melatonin, thyroid hormones, mood, and cognition near the arctic circle, Aviat. Space Environ. Med., 2008, vol. 79, p. 695. 29. Webley, G.E. and Leidenberger, F., The circadian pat tern of melatonin and its positive relationship with progesterone in women, J. Clin. Endocrinol. Metab., 1986, vol. 63, p. 323. 30. Epstein, M.T., McNeilly, A.S., Murray, M.A., and Hockaday, T.D., Plasma testosterone and prolactin in
31.
32.
33.
34. 35.
36.
37. 38.
39. 40.
41.
42.
43. 44.
the menstrual cycle, Clin. Endocrinol., 1975, vol. 4, p. 531. Salonia, A., Pontillo, M., Nappi, R.E., Zanni, G., et al., Menstrual cyclerelated changes in circulating androgens in healthy women with selfreported normal sexual function, J. Sex Med., 2008, vol. 5, p. 854. Salonia, A., Nappi, R.E., Pontillo, M., Daverio, R., et al., Menstrual cyclerelated changes in plasma oxy tocin are relevant to normal sexual function in healthy women, Horm. Behav., 2005, vol. 47, p. 164. Oka, K., Hirano, T., and Noguchi, M., Changes in the concentration of testosterone in serum during the men strual cycle, as determined by liquid chromatography, Clin. Chem., 1988, vol. 34, p. 557. Adam, A., DeLuca, C.J., and Erim, Z., Hand domi nance and motor unit firing behavior, J. Neurophysiol., 1998, vol. 80, p. 1373. Simoneau, J.A., Lortie, G., Boulay, M.R., Thibault, M.S., Thüriault, G., and Bouchard, C., Skeletal muscle his tochemical and biochemical characteristics in seden tary male and female subjects, Can. J. Physiol. Pharma col, 1985, vol. 63, p. 30. Fattorini, L., Felici, F., Filligoi, G.C., Trabbalesi, M., and Farina, D., Influence of high motor unit synchro nization levels on nonlinear and spectral variables of the surface EMG, J. Neurosci. Methods, 2005, vol. 143, p. 133. Stam, C.J. and Reijeveld, J.C., Graph theoretical anal ysis of complex networks in the brain, Nonlinear Bio medical Phys., 2007, vol. 1, p. 3. Longo, G., Montevil, M., and Pocheville, A., From bottomup approaches to levels of organization and extended critical transitions, Front. Physiol., 2012, vol. 3, p. 232. Janse de Jonge, X.A., Effects of the menstrual cycle on exercise performance, Sports Med., 2003, vol. 33, p. 833. Guasti, L., Grimoldi, P., Mainardi, L.T., Petrozzino, M.R., et al., Autonomic function and baroreflex sensitivity during a normal ovulatory cycle in humans, Acta Car diol, 1999, vol. 54, p. 209. Sato, N., Miyake, S., Akatsu, J., and Kumashiro, M., Power spectral analysis of heart rate variability in healthy young women during the normal menstrual cycle, Psychosom. Med., 1995, vol. 57, p. 331. Dimitriev, D.A., Saperova, E.V., Dimitriev, A.D., and Karpenko, Yu.D., The particularities of functioning of the cardiovascular system in different phases of the menstrual cycle, Ros. fiziol. zhurn. im. I.M. Sechenova, Moscow: Sechenova, 2007, vol. 93, issue 3, p. 300. Dunne, F.P., Barry, D.G., Ferriss, J.B., Gearly, G., and Murphy, D., Changes in blood pressure during the nor mal menstrual cycle, Clin. Sci., 1991, vol. 81, p. 515. Moran, V.H., Leathard, H.L., and Coley, J., Cardiovas cular functioning during the menstrual cycle, Clin. Physiol., 2000, vol. 20, p. 496. Translated by N. Shestakova
HUMAN PHYSIOLOGY
Vol. 40
No. 1
2014
