ISSN 03621197, Human Physiology, 2015, Vol. 41, No. 4, pp. 386–393. © Pleiades Publishing, Inc., 2015. Original Russian Text © O.M. Bazanova, N.V. Kholodina, A.Sh. Podoinikov, E.D. Nikolenko, 2015, published in Fiziologiya Cheloveka, 2015, Vol. 41, No. 4, pp. 53–61.
Stabilometric, Electromyographic, and Electroencephalographic Parameters in Postmenopausal Women Depend on Training Support Afferentation O. M. Bazanovaa, c, d, N. V. Kholodinab, c, A. Sh. Podoinikovc, and E. D. Nikolenkoc a
Institute for Prospective Humanitarian Investigations, Sholokhov State University for the Humanities, Moscow, Russia b Novosibirsk State National Research University, Novosibirsk, Russia c Research Institute of Molecular Biology and Biophysics, Siberian Branch, Russian Academy of Sciences, Novosibirsk, Russia d Research Institute of Physiology and Fundamental Medicine, Novosibirsk Russia email:
[email protected] Received August 4, 2014; in final form, December 22, 2014
Abstract—Aging, lack of physical activity, and sedentary lifestyle cause disorders of the sensorimotor inte gration of postural control. The role of support afferentation in changes in the cortical activity in balance impairments has not been studied yet. Changes in the stabilographic (STG) parameters of the body center of gravity, the alpha activity indices of the electroencephalographic (EEG) and electromyographic (EMG) measurements of forehead muscle tone in response to visual activation were studied in standing and sitting positions of postmenopausal women with and without training support afferentation. The variables were compared between three groups: group A (n = 12; age, 66 ± 9 years), women who have purposely been train ing support afferentation using Aikido techniques for the last eight years; group F (n = 12; age, 65 ± 6 years), women who have attended fitness training for the last eight years; group N (n = 11; age, 66 ± 7 years), women who have not engaged in physical exercises for the last eight years. It was found that in group N, a change in the body position from sitting to standing led to a much greater increase in the area of stabilogram and in the energy spent to maintain the balance than in groups A and F. Postural changes from a sitting to standing posi tion increase the tension of forehead muscles and the suppression of α1 amplitude, but decrease the EEG high and lowfrequency αband power and the αband width in group N. In group F, postural changes do not increase the EMG and EEG signs of activation and tension. In group A, standing is accompanied by a decrease in visual activation, psychoemotional tension, and an increase in the α2band power, which is a sign of neuronal efficiency. A conclusion is reached that training focused on support afferentation in postmeno pausal women decreases psychoemotional tension and increases neuronal efficiency of the sensorimotor inte gration of the postural control system and can be used in the prevention of falls in elderly individuals. Keywords: support afferentation sense, posture change, stabilography, EEG αwaves, EMG, postmenopausal women DOI: 10.1134/S0362119715040039
According to the World Health Organization (WHO, 2014) data, the proportion of people over 60 has sharply increased; therefore, the topicality of the active lifestyle of elderly people and prevention of the risk of falls has also increased. Since aging is asso ciated with an impairment of the locomotion system, with a decrease in visual, vestibular, proprioceptive [1] and support [2] systems afferentation and, accord ingly, with disrupted regulation of the processes of sen sorimotor integration of balance maintenance, the risk of falls in elderly people is increasing [3]. In post menopausal women, these processes are aggravated by the estrogen deficit [4]. Note that hormone replace ment therapy does not decrease the falls risk if elderly women are not physically active [5, 6]. In addition,
sedentary lifestyle behavior—a decreased support afferentation—also contributes to the development of disorders of the balance maintenance system [7]. Today, the biomechanical problems of the balance maintenance system have been well studied [8, 9]. It has also been established that in health the balance is maintained not only due to afferentation from visual, vestibular, and proprioceptors [10, 11] but also from the tactile receptors of the foot support zones and, especially, the big toe area [12, 13]. However, the results of the study of the role of support afferentation in the modulation of central mechanisms of voluntary and involuntary regulation of equilibrium have been obtained for either the conditions of weightlessness (or its simulation) [14] or hypergravity [15, 16]. Thus, the
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measurements of αwave activity [17], the most valid index of the central component of sensorimotor inte gration, showed that weightlessness and, conse quently, a decrease in the stimulation of foot support zones, was accompanied by suppression of the EEG αwave power [18], and an increase in support afferen tation under hypergravity of 2–4 g initially increased the αwave power in the 10–12 Hz band with the sub sequent decrease in the amplitude in all the bands of the EEG spectrum [16]. Only in a few studies was the relationship between support afferentation sense and the brain αactivity values studied under the usual conditions of changing position of the body [19–21]. However, the results obtained are contradictory: according to the data of some authors, an increase in support afferentation leads to an increase in power in the α2 band [15] and to a decrease in the coherence of the EEG lowfrequency αwaves with the eyes open (8–10 Hz) [19], and according to the data of other authors, the increase in pressure on foot support zones does not show up in the αactivity changes [20, 21] or even decreases the αwave power [22]. These contra dictions may be explained by different methodological approaches to the measurement of αwave activity. First, this is a frequently used nonindividualized method for assessing αactivity of the brain based on the measurement of only the amplitude values of a cer tain standardized EEG αband [19, 21, 22]. However, the analysis of the EEG power in the frequency bands relative to the individual alpha peak frequency sepa rating the low and upperfrequency αbands allows the typological endophenotypic signs to be identified [23, 24]. For example, for some subjects, the 9–11Hz band may be a highfrequency (at an individual alpha peak frequency of 9 Hz) band; for other subjects, a lowfrequency band (at an individual alpha peak fre quency of 11 Hz) [25]. Second, the results of the assessment of αactivity depend on the experimental conditions, namely, on whether the eyes are closed or open. Since the eyesopen state implies visual activa tion and is accompanied by suppression of the αwave power, it is impossible to compare the dynamics of the αwave amplitude in response to the postural change recorded in the opposite eyesclosed or eyesopen states. Third, the known reciprocal interrelationship between the αwave power and the level of psychoe motional tension assessed by the forehead muscle tone index [26, 27], as well as the EEG contamination by the electromyogram (EMG) lowfrequency and low amplitude waves [28], may lead to misinterpretation of the results of the EEG measurements [26]. Thus, to assess the support afferentation influence on the central component of sensorimotor integration of the balance maintenance system in elderly women, we studied the following characteristics of the EEG αactivity: (1) the αwave power in the individually determined lowfrequency band (this parameter is associated with central processes of involuntary acti vation [24, 29, 30] and involuntary inhibition [31, HUMAN PHYSIOLOGY
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32]); (2) the EEG power in the individually deter mined highfrequency α band whose decrease charac terizes voluntary activation [33, 34] and its increase reflects selective inhibition of irrelevant information [35, 36]; (3) the individual αband width, which reflects the number of frequency generators involved in activation reaction [37] and is associated with non verbal creativity [38]. Simultaneously with the mea surement of the αactivity values, the forehead muscle tone was assessed by electromyography. On the basis of the literature data discussed above, it is possible to propose the hypothesis that purposeful training of support afferentation with the art of Aikido [39, 40] will increase the efficiency of sensorimotor interactions and, as a consequence, decrease excessive activation and psychoemotional tension with a pos tural change in elderly women. Thus, the aim of this work was to study the relation ship between the dynamics of stabilographic, EEG, and EMG values of sensorimotor integration of the balance maintenance system with a change in the body position in elderly women and the support afferenta tion training. METHODS Thirtyfive healthy postmenopausal women whose ages varied between 54 to 78 years took part in the study as volunteers, having signed an informed con sent approved by the Ethics Committee of the Research Institute of Molecular Biology and Biophys ics (Siberian Branch, Russian Academy of Sciences). Women with organic cerebral lesions, marked somatic pathology, or a history of mental diseases, as well as women using psychotropic medications, were not included in this study. Group A (Aikido) included 12 women aged 66 ± 9 years who had been training in Aikido for the past eight years under the supervision of an experienced instructor (Aikido dan 5). One of the main aims of Aikido training is to learn to control sense of load on the plantar support area, especially in the region of the big toe [12, 41] and, as a result, to maintain balance not only in stance, but also during movement perfor mance [39]. For this purpose, the main Aikido instruction is to direct the body weight to the big toes and the anterior part of the foot to ensure the maxi mum contact with the surface and to stimulate the plantar support zones [21, 40]. Group F (Fitness) included 12 women aged 65 ± 6 years with the same experience (at least 8 years) of physical activity (fit ness, yoga, and dancing) as group A women but not aimed at training support afferentation. Group N included 11 agematched women (66 ± 7 years) who had no experience in engaging in physical exercises over the last eight years. The groups were matched by age, occupation, and the percentage of the subjects on hormone replacement drugs.
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After filling in the questionnaire revealing the fea tures of physical activity, health, and the severity of postmenopausal symptoms determined by the Kup perman index in the modification of Uvarova and Vikhlyaeva [42] testing the level of state and trait anx iety [43], simultaneous recording of the stabilogram, electromyogram, and electroencephalogram was per formed under the following experimental conditions: sitting (sitting1) with the eyes closed (EC) for 180 s and with the eyes open (EO) for 60 s; standing with EC for 180 s and with EO for 60 s; and again sitting (sit ting2) with EC for 180 s and with EO for 60 s. According to the standards adopted in posturographic investigations [44], the posture of the subjects in the sitting position was as follows: the head was held straight with a glance in front of themselves, the arms hanging loosely along the sides of the body; the legs bent at the right angle were placed on the stabilo graphic platform; the feet at 35° relative to each other were put on the stabilographic platform according to the marking (their position is not changed with a transfer from the sitting to the standing position) maintaining a pressure of about 20% of the body weight on the platform. The standing posture implies that the subjects stand in a vertical (upright) position. Thus, the influence of the position of the body and EO–EC factors on the measured variables was studied in intergroup comparisons. The capacity for maintaining balance was assessed with stabilography: by the statokinesiogram area (the standard rootmeansquare deviation of the common center of pressure on support along the Х and Y axes (mm2)) and by the calculated energy expenditures rates for maintaining balance, J/s [45]. The stabilo gram was recorded using the ST150 stabilographic platform (Biomera, Moscow). Psychoemotional tension was assessed with EMG measurement of the forehead muscle tone [27] and by the degree of a power decrease in the individually determined EEG αrhythm bands [46]. All the electrophysiological characteristics were recorded and analyzed using the BOSLAB hardware and software device (KOMSIB, Novosibirsk). The EMG was recorded from two bipolar electrodes arranged on the forehead skin; the EEG, from the Pz point in the monopolar montage with a digitalization frequency of 720 Hz in the range 5–50 Hz. The tone of the superficial frontalis muscles was assessed by the EMG integral power value [47]. The analysis of the EEG αwave activity was car ried out with the usual methods for assessing the indi vidual alpha peak frequency and power in the domi nant band, determining the depth of EEG power sup pression in the response to eyes open and the individual width of the αfrequency band [25]. The activation values, namely, the depth of the amplitude suppression in individually determined α1 and α2 bands, were calculated as ln % of a power decrease in
this band in response to eyes open according to the formula ln % = (–100 EO power × 100%)/(EC power). The individual αband width was determined as the part of the EEG frequency spectrum, which includes the frequency bands on the left (the α1band width) and on the right (the α2band width) of the maximal peak frequency and whose spectral power decreases when the eyes are open [25]. Statistical analysis was carried out with the Statis tica software package for Windows using the oneway and multivariate analyses of variance with two factors of withinindividual changes, namely, Body Position (three levels: sitting1, standing, sitting2) and EC– EO (two levels: the eyes closed and the eyes open), and the factor Group (intergroup comparisons; three groups differing in support afferentaion training: A, aikido; F, fitness; N, women with no history of engage ment in physical exercises). RESULTS The comparative analysis of the women’s psycho metric characteristics did not reveal differences in the state and trait anxiety (p > 0.25) in different groups; however, the postmenopausal symptoms assessed by the Kupperman index were the most marked in group N, where the women had no experience in physical exercises (F(2, 112) = 4.3; р = 0.023). The statokinesiogram area and energy spent for maintaining balance in the sitting position, both before and after standing, did not differ in the three groups (p > 0.2). A body position change on standing enlarges the statokinesiogram area and energy spent for balance maintenance in all the subjects (t ≥ 4.56; p ≤ 0.002). However, this increase in groups N and F is greater than in group A (t ≥ 5.12; p ≤ 0.011) (Fig. 1). Note that visual activation (opening the eyes) in the standing position decreases the statokinesiogram area and energy spent for balance maintenance more in group N than in groups A and F (t < –4.79; p < 0.012). Analysis of variance revealed a significant influence of the betweenfactor interaction (Group × Body Position) (F(4, 318) = 2.3; р = 0.005) on the EMG frontal muscle tone values (Fig. 2). This means that the forehead muscle tension with the eyes closed in the sitting1 position (before rising) is higher in group N than in groups A and F (t ≥ 5.23; р ≤ 0.033) and increases still more on standing (t ≥ 7.11; p = 0.001) but decreases on transfer to the sitting2 position (t = –6.12; p = 0.002) (Fig. 2). Visual activation does not increase tonic tension of the forehead muscles in groups A and F in either sitting or standing position (F(4, 318) = 0.78; p = 0.89); and in group N, opening the eyes both in the sitting and standing positions is accompanied by an increase in the EMG power (t = 5.7; р = 0.028). HUMAN PHYSIOLOGY
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In the initial state in the sitting1 position with the eyes closed, the power in the individual α1band did not differ significantly in the three groups. However, upon rising, this value increased in group A (t = 6.2; p = 0.011), did not change in group F, and tended to decrease in group N (t = 2.8; p = 0.061), as a result of which the difference between groups A and N became significant (t = 3.9; p = 0.032). With the subsequent change in the body position from standing to sitting2, the power in the individual α1band returned to the initial level in all the three groups (F(4, 318) = 4.78; p = 0.008) (Fig. 3a). The α2band power in the sitting1 position was the highest in group A (F(2, 96) = 3.78; p = 0.018). Rising increased the α2band power in group A but decreased it in group N and did not change it in group F (F(4, 316) = 4.73; p = 0.005). Returning from the standing to the sitting2 position restored the initial level of the α2power in all the groups (Fig. 3b). Initially in the sitting1 position, the depth of power suppression in response to opening the eyes in HUMAN PHYSIOLOGY
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Fig. 2. Means and standard errors of the electromyogram integral power (μV2) with a change in the sittingstanding sitting position of the body in postmenopausal women. See Fig. 1 for designations.
the α1band was similar in the three groups studied. However, on standing up, this parameter of involun tary visual activation considerably increased in group N, did not change in group F, and decreased in group A (F(4, 316) = 5.79; p = 0.002) (Fig. 4a). A sim ilar dynamics is noted for the power suppression depth in the α2band with a change in the body position (sit ting1, standing, sitting2): in the initial sitting1 posi tion, this parameter of voluntary activation is higher in group N than in groups F and A (t = 6.45, p = 0.001); standing up increases activation of α2waves in groups N and F, but decreases it in group A (F(4, 316) = 6.18; p = 0.001) (Fig. 4b). The width of the EEG frequency band where sup pression of the αwave amplitude occurs in response to eyes open is also equal in the groups in the sitting1 position but narrows in groups N and F and widens in group A (F(4, 316) = 8.19; p = 0.0001) in standing
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results agree with the concepts of other authors that physical activity training decreases psychoemotional tension and anxiety in elderly individuals [52, 53] and might explain the decrease in the markedness of post menopausal symptoms in groups A and F observed by us. According to the known data that an increase in the EMG scalp muscle power indicates an increase in psy choemotional tension [26], it may be asserted that standing up is a stressful factor for women of a seden tary lifestyle behavior. However, the results of stabilo graphic and electromyographic studies give evidence of only nonspecific influence of physical exercises on the psychophysiological system of balance mainte nance on the whole, without emphasizing the impor tance of support afferentation.
The results of this study demonstrate an alleviation of postmenopausal symptoms in groups A and F, which gives additional proof of an undisputable role of physical exercises for elderly individuals and their importance in the prevention of falls [48]. Note that this study has been the first to find that the statokine siogram area and energy expenditure for balance maintenance in the standing position are the highest in women lacking experience in physical exercises (Fig. 1). This is not surprising, because destabilization of the upright position of the body is related not only to aging [49, 50], but predominantly to the sedentary lifestyle of these women [7, 51]. In addition, rising up increases their forehead muscle tone to a greater degree than in physically active women (Fig. 2). These
In order to determine the role of support afferenta tion in sensorimotor integration of balance mainte nance, we compared the results of the study of women with a similar level of physical activity but differing in the degree of training support afferentation. It appeared that the increase in the average level of energy spent for balance maintenance and the scalp muscle activation on rising is greater in group F women than in the women purposefully training sup port afferentation (Figs. 1, 2). In addition, opening the eyes, i.e., an increase in visual afferentation playing one of the key roles in the system of balance mainte nance [54], increases postural stability (decreases the statokinesiogram area) only in group F and group N women but does not change it in group A. This means
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Fig. 3. Means and standard errors of the EEG power in individual (a) α1 and (b) α2 bands (μV2) with a change in the sittingstandingsitting position of the body in post menopausal women. See Fig. 1 for designations.
position (Fig. 4b). Returning to the sitting2 position the αband width narrows in group A (t = –5.45, p = 0.032) but increases in groups N and F (t ≥ 6.35, p ≤ 0.008) (Fig. 4c).
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that purposeful training of support afferentation mod ifies the mechanism of regulation of balance mainte nance so that the role of visual activation becomes less important. To test this hypothesis, we compared the results of measurements of the values of the cerebral α activity as a central component of the system of visual activation. It appeared that, as judged by the αwave amplitude suppression value in response to opening the eyes [30, 46], visual activation was the highest precisely in group N in the standing position, whereas for women purposefully training their support afferentation, the decrease in the EEG αwave amplitude in response to opening the eyes was not significant. That the increase in support afferentation may decrease the role of visual activation in balance maintenance was also confirmed by the results of Vecchio et al. [55], who showed that the role of visual activation in sensorimotor integra tion decreased in masters of shooting purposefully training proprioceptive and tactile sensitivity of sup port afferentation zones [55]. Additional proof that group A women have less dif ficulty maintaining balance than group F and group N is the data obtained when the width of the frequency band (where the activation–suppression of the αwave amplitude occurs in response to opening the eyes) is not decreased in standing. Upon standing up, the α band widens only in group A, but narrows in groups F and N. Assuming that the frequency band widening indicates an increase in the number of the frequency generators involved in activation [37], we may suggest that training support afferentation facilitates the switching of the processes of bioelectrical impulses generation in the central nervous system [56], thus increasing the plasticity of neuromuscular interactions [14]. When the power of highfrequency αwaves as a characteristic of the inhibition was studied [23, 29, 35], this parameter appeared to be considerably higher in the group of women training support afferentation than in groups F and N, even in the sitting position. Note that standing up increases the αwave power only in group A but decreases or does not change it in women who do not train support afferentation. This leads us to suggest that purposeful training of support afferentation increases neuronal efficiency and, as a consequence, the efficiency of sensorimotor integra tion in the balance maintenance system. Insufficiency of the support afferentation is a trigger in the develop ment of the complex of psychophysiological disorders. In other words, Aikido training aimed to learning movement with balance maintenance by activating plantar support zones decreases the cost of vertical position of the body maintenance and its dependence on visual activation. Summing up the results obtained, we may conclude that the absence of any physical exercises in post menopausal women decreases the stability of the verti cal position of the body, increases psychoemotional HUMAN PHYSIOLOGY
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tension and the load on the visual analyzer, while pur poseful training of support afferentation compensates the disorders related to age and sedentary lifestyle by increasing the sensorimotor integration effectiveness, thus facilitating the processes of balance maintenance regulation. ACKNOWLEDGMENTS This study was supported by the Russian Founda tion for Humanitarian Research, project no. 1406 00951a. REFERENCES 1. Lee, H.J. and Chou, L.S., Detection of gait instability using the center of mass and center of pressure inclina tion angles, Arch. Phys. Med. Rehab., 2006, vol. 87, p. 569. 2. Barrett, R.S., Mills, P.M., and Begg, R.K., A system atic review of the effect of ageing and falls history on minimum foot clearance characteristics during level walking, Gait Posture, 2010, vol. 32, no. 4, p. 429. 3. Lord, S.R., Menz, H.B., and Tiedemann, A., A physi ological profile approach to falls risk assessment and prevention, Phys. Ther., 2003, vol. 83, no. 3, p. 237. 4. Nedergaard, A., Henriksen, K., Karsdal, M.A., and Christiansen, C., Musculoskeletal ageing and primary prevention, Best Pract. Res. Clin. Obstet. Gynaecol., 2013, vol. 27, no. 5, p. 673. doi: 10.1016/j.bpob gyn.2013.06.001. 5. Naessen, T., Lindmark, B., Larsen, H.C., et al., Tibolone low dose (1.25 mg/d) therapy and postural balance in elderly women, Maturitas, 2009, vol. 62, no. 1, p. 72. 6. Lee, I.H. and Park, S.Y., Balance improvement by strength training for the elderly, J. Phys. Ther. Sci., 2013, vol. 25, no. 12, p. 1591. doi: 10.1589/jpts. 25.1591. 7. KesseGuyot, E., Andreeva, V.A., Lassale, C., et al., Clustering of midlife lifestyle behaviors and subsequent cognitive function: a longitudinal study, Am. J. Public Health, 2014, vol. 104, no. 11, p. e170. 8. Gurfinkel’, V.S., Kots, Ya.M., and Shik, M.L., Regu lyatsiya pozy cheloveka (Regulation of Human Pos ture), Moscow: Nauka, 1965. 9. Bernshtein, N.A., Fiziologiya dvizhenii i aktivnost’ (Physiology of Movements and Activity), Moscow: Nauka, 1990. 10. Carpenter, M.G., Allum, J.H., and Honegger, F., Directional sensitivity of stretch reflexes and balance corrections for normal subjects in the roll and pitch planes, Exp. Brain Res., 1999, vol. 129, no. 1, p. 93. 11. Honeine, J.L. and Schieppati, M., Timeinterval for integration of stabilizing haptic and visual information in subjects balancing under static and dynamic condi tions, Front Syst. Neurosci., 2014, vol. 8, p. 190. doi: 10.3389/fnsys.2014.00190. 12. Mickle, K.J., Munro, B.J., Lord, S.R., et al., Gait, bal ance, and plantar pressures in older people with toe deformities, Gait Posture, 2011, vol. 34, no. 3, p. 347.
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Translated by E. Babchenko
