ISSN 03621197, Human Physiology, 2014, Vol. 40, No. 4, pp. 375–382. © Pleiades Publishing, Inc., 2014. Original Russian Text © O.M. Bazanova, O.I. Kuzminova, E.D. Nikolenko, S.E. Petrova, 2014, published in Fiziologiya Cheloveka, 2014, Vol. 40, No. 4, pp. 27–35.
EEG Activation Response under Different Neurohumoral States O. M. Bazanovaa, b, O. I. Kuzminovac, E. D. Nikolenkob, and S. E. Petrovab a
Russian Institute for Advanced Study in Humanities and Technology, Sholokhov Moscow State University for the Humanities, Moscow, 109240 Russia b Institute of Molecular Biology and Biophysics, Siberian Branch, Russian Academy of Medical Sciences, Novosibirsk, 630117 Russia c Research Center for Clinical and Experimental Medicine, Siberian Branch, Russian Academy of Medical Sciences, Novosibirsk, 630117 Russia email:
[email protected] Received August 8, 2013
Abstract—In order to determine under which neurohumoral conditions the response to usual opening of the eyes stimulates the Berger effect, the electroencephalographic, electrocardiographic, and electromyographic responses to eyes opening have been recorded simultaneously with the psychometric indices of emotional tension and cognitive performance in 59 healthy women aged 18–27 years every two or three days during one or two menstrual cycles determined according the progesterone level in the morning. For excluding the influ ence of the Novelty factor, the monitoring began at the menstrual phase of the cycle in 29 women and at the luteal phase in the other 30 women. A single examination has been performed in a separate group of 30 women to study the relationship of these parameters with the current progesterone and cortisol levels in saliva. Two factor ANOVA has shown that the magnitude of amplitude suppression and the bandwidth of the lowfre quency α EEG range in the follicular phase of the menstrual cycle are greater than in the luteal one and depend on the Novelty factor. The indices of the Berger effect of the upperfrequency α range do not depend on the neurohumoral state or the Novelty factor. The amplitude suppression and the bandwidth of the low frequency α range alone are predictors of the activation in the response to eyes opening because the changes are unidirectional and are interrelated with the autonomic and hormonal characteristics of the activation. It has been demonstrated that eyes opening is a stimulus for the activation only in the neurohumoral state cor responding to the follicular phase of the menstrual cycle. This study has established the dependence of the central and autonomic activation on the individual α frequency EEG profile and the neurohumoral state. Keywords: activation, eyes opening, magnitude and duration of EEG αwave suppression, individual αpeak frequency, individual alpha bandwidth, neurohumoral state DOI: 10.1134/S0362119714040045
Study of the dependence of higher nervous system activity on the type of neurohumoral regulation is one of the main fundamental tasks of psychophysiology. Numerous data have been accumulated on the indi vidual response of psychophysiological systems to stress. However, there are much fewer published stud ies on the psychophysiological characteristics that could be served as indices of the activation response, a specific adaptive response of the body to nonstressor everyday stimuli, reflecting the transition from relative rest to activity. Until recent time, the activation response was only estimated from the changes in phys iological characteristics, such as an increased skin conductance [1, 2], heart and respiration rates [3], tonic muscle tension [4], a shortterm increase in the free cortisol level [5], and an increased blood oxygen ation level of the brain [6]. Changes in the bioelectric processes in the brain, which are direct neuronal acti vation indices, were not taken into account. Barry et al. [1] suggested that the standard reaction of the αwave EEG suppression in response to eye
opening or the socalled Berger effect should be used for identification of the neuronal activation. Studies of the past decade have yielded much evidence for the involvement of the Berger effect parameters in neu ronal inhibition and excitation [1, 7–9]. For example, the decrease in the amplitude is correlated with the intensity of activation [1], and the duration of decay of this response reflects the lability/stability of neuronal processes [9]. The width of the α band in which the amplitude is decreased serves as an index of the vari ability of generators of different frequencies and reflects the capacity for refocusing and the creativity in solving cognitive tasks [10, 11]. The power of the acti vation response depends on sociopsychological factors [12, 13] and the initial activation level or arousal of the individual. For example, empirical studies have shown that the activation is less pronounced in subjects with an enhanced anxiety [12] or attention deficit [13] than in healthy subjects. On the other hand, the intensity of the activation response depends on the initial arousal according to the Yerkes–Dodson law: if the initial
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body activation is very high or very low, then the acti vation intensity is small [14]. It has been recently dem onstrated that the αfrequency pattern of brain bio rhythms also affects the activation response [7, 8]. The highfrequency (≥10 Hz) and lowfrequency ( 0.78). The actual cortisol level in saliva sampled shortly before the electrophysi ological measurements in the state of rest with the eyes closed did not depend on the cycle phase or the Start of Monitoring factors [F(4,507) < 0.97]. The cortisol level in saliva sampled in the eyes opening rest condi tion within 5 min was the highest in the FP [F(4,507) = 4.52; р = 0.005]. In this period, the cortisol level in the rest eyes open condition was higher compared to the EC condition (t ≥ 4.67, p ≤ 0.021). The number of correct responses in test for spatial imagination (the Mental Rotation Task) and the flu ency of backward count were the greatest in the LP [F(4,503) ≥ 4.48; р ≤ 0.015, LP vs. PMP, MP (t ≥ 4.7, p ≤ 0.04)] and did not depend on the moment when monitoring started [F(4,504) = 1.52; р ≥ 0.28]. The degree of psychoemotional tension determined by the Wolneffer coefficient of the Lüscher color test and the state anxiety index were the lowest in the LP [F(4,302) = 5.38; р ≤ 0.011]. The degree of psychoemotional tension deter mined by the EMG amplitude of muscle frontalis was
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the lowest in the LP and the highest in the MP and PMP [LP vs. OP (t ≥ 4.1, р ≤ 0.04) and LP vs. PMP (t ≥ 6.5; р ≤ 0.02)] [F(4,501) ≥ 5.17, р ≤ 0.01], with the heart rate (HR) not changing significantly. The largest increase in both the EMG amplitude and HR in response to eyes opening was observed in the FP (t ≥ 5.28, p ≤ 0.01 EC vs. EO). The magnitude of amplitude suppression in the α1 band in response to eyes opening (Fig. 3a) was the greatest in the FP [FP vs. MP, OP, LP, PMP (p ≤ 0.05)]. The power suppression in the α1 band during the MP was greater in the group whose monitoring started in the same phase than in the group whose monitoring started at the LP (t ≥ 5.6, p ≤ 0.021). Con versely, this suppression during the LP was greater in the group whose monitoring started in the LP than in the group whose monitoring started in the MP (t ≥ 4.8, p ≤ 0.032). The ovarian hormonal cycle phase change and the Start of Monitoring factors did not affect the magni tude of power suppression in the α2 band (Fig. 3b). The duration of the Berger effect in the α1 band was the longest in the LP [LP vs. MP, FP, OP, PMP] [F(4,507) ≥ 6.10, р ≤ 0.01] (Fig. 4a); in the α2 band, it did not vary during the cycle (Fig. 4b). In neither band was this index affected by the Start of Monitoring factor. Pairwise comparisons showed that the α1 band was wider during the FP and OP than during the LP and PMP (t ≥ 4.5, p ≤ 0.05) (Fig. 5a), whereas the α2 band was the widest during the LP [(t ≥ 6.1, p ≤ 0.01) LP vs. MP, FP, OP, PMP] (Fig. 5b). Correlation analysis of the data on the actual hor mone levels in saliva and psychometric characteristics showed that the progesterone level was positively cor
related with the cognitive performance index (the flu ency of backward count) (r ≥ 0.81, p ≤ 0.001) and neg atively correlated with the index of psychoemotional tension (the Wolneffer coefficient of the Lüscher test) (r ≥ –0.67, p ≤ 0.004), state anxiety level (r ≥ –0.58, p ≤ 0.011), and integral EMG power (r ≥ –0.53, p ≤ 0.011). The cortisol level was positively correlated with the state anxiety level (r ≥ 0.62, p ≤ 0.005) and HR (r ≥ 0.56, p ≤ 0.010). The increase in the cortisol level in response to eyes opening was negatively correlated with the number of correct replies in the Mental Rotation Task (r ≥ –0.42, p ≤ 0.031) and backward count fluency (r ≥ –0.44, p ≤ 0.026) and positively correlated with the increase in the integral EMG power (r ≥ 0.55, p ≤ 0.010) and the increase in HR (r ≥ 0.43, p ≤ 0.025). The results of the correlation analysis of the rela tionship of the Berger effect characteristics with the actual hormone levels in saliva, psychometric parame ters, and electrophysiological parameters showed that the magnitude of amplitude suppression in the α1 band was positively correlated with the increases in the musclefrontalis tension (r ≥ 0.45, p ≤ 0.04), cortisol level (r ≥ 0.61, p ≤ 0.01), and HR (r ≥ 0.42, p ≤ 0.02) in response to eye opening. Note that the duration of the power suppression in the α1 band was correlated with the psychometric index of state anxiety (r ≥ 0.52, p ≤ 0.01), whereas the width of the α1 band, conversely, was nega tively correlated with this anxiety index (r ≥ –0.42, p ≤ 0.02). The correlation analysis also showed the depen dence of the Berger effect characteristics in the α1 band on the progesterone level: the magnitude and duration of power suppression were, respectively, neg atively (r ≥ –0.78, p ≤ 0.01) and positively (r ≥ 0.68, p ≤ 0.01) correlated with the level of this hormone. In the α2 band, only one characteristic of the Berger effect, namely the bandwidth, was related to the hor monal and psychometric parameters: it was positively correlated with the progesterone level (r ≥ 0.67, p ≤ 0.01) and the number of correct replies in the Mental Rotation Task (r ≥ 0.48, p ≤ 0.02). DISCUSSION The ovarian hormonal cycle in women was used as a model of natural variation of the neurohumoral state [18] because the endogenous progesterone level changes by four to five times during the cycle [23]. In this study, progesterone, which modulates the trans mission and inhibition of nerve impulses [35, 36], served as the main factor forming different psycho physiological states and determining the activation level. Indeed, our experimental model allowed us to compare the psychophysiological indices of activation at neurohumoral states differing in the progesterone level by a factor of three to five. As expected, the cog nitive performance was the highest, and emotional tension the lowest, in the LP of the cycle, when the progesterone level peaked. HUMAN PHYSIOLOGY
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Fig. 3. Mean values and errors of the mean of the degree of power suppression (ln%) in the (a) α1 and (b) α2 bands during different phases of the ovarian hormonal cycle in the groups of women in which monitoring started in the menstrual and luteal phases. # Significant difference (p < 0.05) between the groups. The abbreviations here and in Figs. 4 and 5 are explained in the “Experi mental.”
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Fig. 4. Mean values and errors of the mean of the calculated duration (s) of the Berger effect in the (a) α1 and (b) α2 bands during different phases of the ovarian hormonal cycle in the groups of women in which monitoring started in the menstrual and luteal phases.
We found that the magnitude of power suppression and the width of the α band in its lowfrequency part alone varied unidirectionally and was correlated with the autonomic and hormonal parameters of activation and orientation response depending on the neurohu moral state. Specifically, during the FP, when the power suppression in the α1 band was the greatest, the increases in the EMG amplitude and HR in response to eyes opening were the greatest, whereas during the LP, when the progesterone level peaked, the smallest power suppression in the α1 band and the weakest emotional tension were observed. The magnitude of the α1 band power suppression was the most sensitive to the Novelty and Start of Monitoring factors, which confirms that the magnitude of amplitude suppression in the individual lowfrequency α1 band could serve as a marker of the intensity of activation response. Thus, the neurohumoral state in the FP facilitates the activation response as judged by the EMG, HR, HUMAN PHYSIOLOGY
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and hormonal parameters, as well as by the magnitude of α power suppression, and the state during the LP creates the conditions for the lowest reactivity to non stressor stimuli. The power suppression in the lowfre quency α band may be regarded as an index of the intensity of the activation in response to eyes opening. In other words, we have demonstrated that, in addition to the previously known physiological and psychometric estimates of the activation level, there is one more reliable and easily measurable index of neu ronal activation, namely, the EEG power suppression in the individually determined lowfrequency α band. At the same time, the duration of the Berger effect in the α1 band has proved to be the longest in the state characterized by the highest progesterone level and not correlated with physiological indices of activation, including the cortisol level and HR. Apparently, the duration of the Berger effect in the α1 band reflect cerebral processes other than activation. For example,
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Fig. 5. Mean values and errors of the mean of the widths of the (a) α1 and (b) α2 bands during different phases of the ovarian hormonal cycle in the groups of women whose monitoring started at the menstrual and luteal phases.
according to Golubeva [9], stability of the response to eyes opening indicates inhibition of the activation pro cesses that are insignificant for information process ing, which is usually related to an increase in cognitive performance [37]. Thus, the characteristics of the Berger effect in the lowfrequency α band play different roles. During the FP, the magnitude of α1 power suppression serves as an index of activation; conversely, during the LP, when the progesterone level is increased, the duration of this suppression may reflect inhibition of cortical pro cesses. Regarding the individual upperfrequency α band, neither the magnitude nor the duration of power sup pression changes with the change in the neurohumoral state; nor are they affected by the Novelty factor or correlated with autonomic parameters of activation. Therefore, the magnitude and duration of the power suppression in the highfrequency α band cannot be regarded as predictors of activation. The bandwidth of the frequency range in which the power suppression occurs, an α wave parameter that is rarely analyzed, also changes depending on the neuro humoral state. Specifically, the α2 bandwidth is the highest at the highest progesterone level, i.e., during the LP; that of the α1 band, during the OP. Since wid ening of the range in which desynchronization occurs means an increase in the diversity of frequency gener ators involved in the activation response [8, 38], it could be concluded that the OP is characterized by an increase in the number of lowfrequency generators and, hence, widening of the α1 band caused by estro gen, and the LP is characterized by an increase in the number of highfrequency α generators and widening of the α2 band with increasing progesterone level. We can assume that the widening of the lowfrequency α band characterizes the activation of perception pro cesses, which has been reported to be stimulated with
estrogen [39–41]. Indeed, according to the results of our previous study, women exhibit the highest auditory and tactile sensitivities during the FP [17, 42]. In turn, the widening of the α2 frequency band may be deter mined by an increase in the progesterone level, which increases the variation of precisely highfrequency impulses [35]. In addition, an increase in the progest erone level is known to be accompanied by intensifica tion of switchover processes [36] and the resultant increase in cognitive performance [11]. Indeed, we recorded the best cognitive performance and the larg est α2 bandwidth for the neurohumoral state with the highest progesterone level; moreover, the former two parameters were positively correlated with each other. These data constitute further evidence for the assump tion [43, 44] that the indices of power suppression in different α frequency bands are related to different psychophysiological functions. Thus, the results of this study demonstrate a differ ence between the mechanisms of neuronal activation in the low and highfrequency individual α bands. Analysis of our results leads to the conclusion that the characteristics of the psychophysiological response to eyes opening change depending on the neurohumoral state related to the progesterone level. The activation response is more intense in the neuro humoral state with a low progesterone level and low α frequency than in the state with a high progesterone level and high α frequency. Since the changes are uni directional and interrelated with the autonomic and hormonal characteristics of activation, only two of the Berger effect indices, the magnitude of power suppres sion and the width of the lowfrequency α band are reliable predictors of the activation response. HUMAN PHYSIOLOGY
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CONCLUSIONS An increased power suppression and a widened individual lowfrequency α band related to increases in the psychoemotional tension, HR, and cortisol level in response to eyes opening are indices of the activa tion response. The psychophysiological characteristics of the acti vation response are the most marked in the neurohu moral state with a low progesterone level correspond ing to the FP of the ovarian hormonal cycle in women. The magnitude and duration of power suppression in the individual upperfrequency α band are recip rocally related to cognitive performance indices, and the width of the band is directly proportional to these indices. The intensity of psychophysiological activation processes depends on the neurohumoral state and the individual αfrequency EEG pattern. Study of the activation level changes during the ovarian hormonal cycle in women adds to our knowl edge on the mechanisms of neural–visceral relation ships. These data can be used in developing the meth ods for diagnosing stress states and correcting post stress disorders, predicting the success of treatment, and preventing and treating mental disorders. These data can serve as a basis for protocols of psychotherapy (neurofeedback) taking into account individual bio rhythm patterns of women.
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