ISSN 03621197, Human Physiology, 2014, Vol. 40, No. 4, pp. 375382. 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. 2735.

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: bazanova@soramn.ru
Received August 8, 2013

AbstractIn 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 1827 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 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 range do not depend
on the neurohumoral state or the Novelty factor. The amplitude suppression and the bandwidth of the low
frequency 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 frequency EEG profile and the neurohumoral state.
Keywords: activation, eyes opening, magnitude and duration of EEG wave suppression, individual peak
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 wave 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, 79]. 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 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 YerkesDodson law: if the initial

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BAZANOVA et al.

body activation is very high or very low, then the acti

vation intensity is small [14]. It has been recently dem
onstrated that the frequency pattern of brain bio
rhythms also affects the activation response [7, 8]. The
highfrequency (10 Hz) and lowfrequency (<10 Hz)
EEG oscillators have proved to be differentially
involved in the activation response [7, 8]. Similarly,
Tenke et al. [15] have shown that the metabolic activa
tion of the brain (the blood oxygenation level) upon
eyes opening is more clearly reflected in the lowfre
quency EEG band than in the highfrequency one.
To date, the dependence of the activation response
on the neurohumoral state has been demonstrated
only for the extreme change in the hormone levels
caused by stress [5, 16]. The relationship of activation
with the normal neurohumoral background has hardly
been studied at all. Therefore, the effect of the natural
variation of the endogenous hormone levels is rarely
taken into account in psychophysiological studies
[17]. At the same time, the ovarian/menstrual cycle in
women may serve as an ideal model for studying the
relationship between the natural variation of the neu
rohumoral state and the psychophysiological charac
teristic of activation [18]. Our previous study has dem
onstrated changes in psychophysiological parameters
during the menstrual cycle [17], which is known to
result from the changes in the levels of hormones, in
particular, steroids affecting the neuronal activity, such
as progesterone [19, 20] and estrogens [21].
In this study, in order to estimate the dependence of
the psychophysiological parameters of activation on
the neurohumoral state, we set the following tasks:
analyzing the relationship between autonomic, hor
monal, neuronal, and psychological characteristics of
the activation response as dependent on the fre
quency range and the phase of the ovarian hormonal
cycle in women and determining in which neurohu
moral state eye opening is a stimulus for the activation
response.
METHODS
Eightynine female volunteers aged 18 to 27 years
participated in the study. All of them gave their
informed written consent in the form approved by the
Ethics Committee of the Institute of Molecular Biol
ogy and Biophysics of the Siberian Branch of the Rus
sian Academy of Medical Sciences. At the time of the
study, all the women were apparently healthy, not dis
playing symptoms of somatic or mental diseases, and
took no hormonal or psychotropic drugs for six
months before the study or during the study.
According to standards [22], a menstrual cycle was
divided into five phases, which were identified individ
ually: the menstrual phase (MP, from the first to the
last days of bleeding); the follicular phase (FP, from
the day after the end of bleeding to the start of basal
temperature raise by 0.51C); ovulatory phase (OP,
from the first day of basal temperature raise to the first

day of an increase in the free progesterone content of

saliva by more than 20%); luteal phase (LP, from the
first day of an increase in the salivar progesterone level
to the start of its decrease by more than 20%); and pre
menstrual phase (PMP, from the first day of the
decrease in progesterone level to the start of menstru
ation).
Samples of saliva of 59 women examined every two
or three days during the menstrual cycle (1417 times)
were taken two times during every day of examination:
in the morning, on an empty stomach (for determin
ing the cycle phase) and in the evening, together with
the monitoring of psychophysiological indices. The
monitoring was performed from 6 p.m. to 10 p.m. in
the rest state with the eyes closed and open. Another
30 women participated in a single examination. The
psychometric testing and sampling of saliva for analyz
ing the actual progesterone and cortisol levels were
performed in parallel with the recording of EEG, elec
trocardiogram (ECG), and electromyogram (EMG).
For determining the change in the actual salivar corti
sol level in response to the eyes opening, saliva was
sampled in the state of rest after 5 min of the subject
being at rest with the eyes closed and 12 min after she
opened her eyes.
In order to exclude the effect of habituation to the
experimental conditions and estimate the effect of the
Novelty factor (orientation response), the monitoring
started at the beginning of the menstrual phase in 30
subjects and in the middle of the cycle, after the basal
temperature raise, in 29 subjects.
Thus, the experiment was designed so as to esti
mate the effects of the following factors: the within
individual factors Cycle Phase at five levels (MP, FP,
OP, LP, and PMP) and Eyes Opening at two levels
(eyes closed and eyes open) and the betweengroup
factor Start of the Monitoring; i.e., we compared
two groups of women: group 1 that started monitoring
in the MP and group 2 that started monitoring in the
LP. The salivar progesterone and cortisol levels were
determined using ELISA [23].
Psychometric estimation of emotional tension was
carried out using the Wolneffer coefficient of the
Lscher color test [24] and state anxiety level [25], as
well as the change in the superficial muscle frontalis
tone [26] and heart rate [27, 28]. The mental backward
count test was used to estimate the fluency of cognitive
task solution. We also used the Mental Rotation Task
as a test for spatial imagination [29]. It effectiveness
was calculated as the number of correct responses per
unit time.
The muscle frontalis tension was measured using
EMG recorded with a sampling rate of 720 Hz. The
heart rate was estimated by the frequency of the R
wave in ECG recorded from three cardiographic elec
trodes located according to the simple Einthoven tri
angle system [30]. The EMG, ECG, and EEG were
recorded using a BOSLAB hardwaresoftware system
(Novosibirsk, Russia). The EEG was recorded
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EEG ACTIVATION RESPONSE UNDER DIFFERENT NEUROHUMORAL STATES

through the Pz monopolar derivation (according to

the international 1020 system) in the bandpass of
0.350 Hz at a sampling rate of 720 Hz. We used the
Pz site because the previous study showed that the
rhythm characteristics recorded from the parieto
occipital area were the most stable and reproducible
[31, 32]. For eliminating motor artifacts, we used the
individual component analysis (ICA) method whose
algorithm is included in the BOSLAB software.
The individual alphapeak frequency was deter
mined from the spectral analysis of a 1min EEG
epoch recorded in the state of rest with the eyes closed
(EC). For calculating the magnitude of amplitude
suppression and the individual alpha bandwidth, we
used the last 20 s of the EC state and the first four 5s
epochs of EEG in the eyes open (EO) state. Four con
secutive EEG epochs recorded in the EO state were
used for calculating the Berger effect decay: 05, 6
10, 1115, and 1620 s. All EEG periods were pro
cessed using the fast Fourier transform (FFT) in the
band of 320 Hz with the use of the Hann window and
compared with the results of the spectral analysis of
the last 20 s of EEG recorded in the EC state. As a
result, we determined the individual boundaries of the
1 and 2 frequency bands [11]. Correspondingly, the
spectral power (V2) and power suppression (ln%)
were determined for the individually identified 1 and
2 bands (Fig. 1). The magnitude of amplitude sup
pression was estimated from the equation [33]
EO power 100%
ln% = .
EC power
The EEG amplitude decreases at the moment of
eyes opening and is, gradually, partly restored after
wards [9, 34]. For calculating the duration of the
Berger effect, we used the equation for the arctg
function, where X = 0, 5, 10, 15, 20 s; and Y is the
magnitude of power suppression in these periods (in
ln%). First, we calculated the arctg (in radians) of
the angle between the tangent line of the function of
power decrease with time and the abscissa axis. Then,
the following equation was used:
ln(100%)/tan = 4.61/tan .
The Statistica software was used for statistical treat
ment. One and twofactor ANOVA was performed
for the factors of withinindividual changes Cycle
Phase (five levels; in the cases of post hoc compari
sons involving the calculation of the Sheffe coeffi
cient) and Eyes Opening (two levels) and the factor
of betweenindividual comparisons Start of Moni
toring (monitoring started in the MP and LP).
Correlation analysis using Spearmans coefficient
was performed for determining the relationships
between the psychometric, electrophysiological, and
hormonal parameters.
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377

V2
15
10

Amount of power suppression

Frequency of the maximum peak

0
3

TF

11 BF 13
2

15

17

19Hz

band width

Fig. 1. EEG spectral power in the Pz electrode derivation

in the state of rest with the eyes closed (the solid line) and
open (the dashed line). The spectral power that is more
than 20% lower than the baseline level is taken to belong to
the individual band (between points TF and BF), which
are the points at which the spectral curve in the eyesclosed
state intersects the spectral curve in the eyesopen state.
Individually determined 1 and 2 bands are indicated on
the abscissa axis. The abscissa shows the frequency (Hz);
the ordinate shows the spectral power (V2).

RESULTS
The repetitive ANOVA analysis showed a statistical
homogeneity of the progesterone level of the saliva
sampled in the morning, on an empty stomach from
day 1 to day 20 2, its increase between days 21 3
and 26 1 (LP), and its decrease on day 27 1 of the
cycle [F(4,507) = 6.54; < 0.001] (Fig. 2).
Similarly, the progesterone level recorded at the
moment of the psychophysiological study in women
that were in the postovulatory LP was higher com
pared to the MP and preovulatory phase [F(4,509) =
5.51; < 0.001]. The mean progesterone concentra
tions in saliva sampled in the EC and EO states did not
differ from each other ( > 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; = 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; 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; 0.28]. The
degree of psychoemotional tension determined by the
Wolneffer coefficient of the Lscher color test and the
state anxiety index were the lowest in the LP [F(4,302) =
5.38; 0.011].
The degree of psychoemotional tension deter
mined by the EMG amplitude of muscle frontalis was

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BAZANOVA et al.

pg/mL
450

ng/mL
45

400

40

350
300

35
*

30

250
200

25
*

20

150

15

100

10

50

0
1 3 5 7 9 11 13 15 17 19 21 23 25 27 29
Days of the cycle

Fig. 2. Mean values and errors of the mean of the progest

erone (the black line and the left ordinate axis) and cortisol
(the gray line and the right ordinate axis) concentrations in
saliva sampled from 59 women in the morning during the
ovarian hormonal cycle. Here and in Figs. 3, 4, and 5,
* significant difference (p < 0.05) between phases of the
cycle.

the lowest in the LP and the highest in the MP and

PMP [LP vs. OP (t 4.1, 0.04) and LP vs. PMP (t
6.5; 0.02)] [F(4,501) 5.17, 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 1
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 1 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 2 band (Fig. 3b).
The duration of the Berger effect in the 1 band was
the longest in the LP [LP vs. MP, FP, OP, PMP]
[F(4,507) 6.10, 0.01] (Fig. 4a); in the 2 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 1 band was
wider during the FP and OP than during the LP and
PMP (t 4.5, p 0.05) (Fig. 5a), whereas the 2 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 Lscher 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 1
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 1 band was correlated with the
psychometric index of state anxiety (r 0.52, p 0.01),
whereas the width of the 1 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
1 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 2 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.
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ln %
2.0

ln %
2.0

(a)

1.8
1.6
1.4

379

(b)

1.8
1.6

1.4
MP FP OP LP PMP
MP FP OP LP PMP
Phase of the cycle
Phase of the cycle
Monitoring started in the MP
Monitoring started in the LP

Fig. 3. Mean values and errors of the mean of the degree of power suppression (ln%) in the (a) 1 and (b) 2 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.

s
25

(a)

s
25
20

(b)

20

15

15

10

10

5
MP FP OP LP PMP
MP FP OP LP PMP
Phase of the cycle
Phase of the cycle
Monitoring started in the MP
Monitoring started in the LP

Fig. 4. Mean values and errors of the mean of the calculated duration (s) of the Berger effect in the (a) 1 and (b) 2 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 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 1 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 1 band and the weakest
emotional tension were observed. The magnitude of
the 1 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 1 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,
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and hormonal parameters, as well as by the magnitude

of 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 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 band.
At the same time, the duration of the Berger effect
in the 1 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 1 band reflect
cerebral processes other than activation. For example,

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BAZANOVA et al.
Hz
6

(a)

Hz
6

(b)

1
MP FP OP LP PMP
MP FP OP LP PMP
Phase of the cycle
Phase of the cycle
Monitoring started in the MP
Monitoring started in the LP

Fig. 5. Mean values and errors of the mean of the widths of the (a) 1 and (b) 2 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 band play different roles. During the
FP, the magnitude of 1 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 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 band cannot be
regarded as predictors of activation.
The bandwidth of the frequency range in which the
power suppression occurs, an wave parameter that is
rarely analyzed, also changes depending on the neuro
humoral state. Specifically, the 2 bandwidth is the
highest at the highest progesterone level, i.e., during
the LP; that of the 1 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 1 band caused by estro
gen, and the LP is characterized by an increase in the
number of highfrequency generators and widening
of the 2 band with increasing progesterone level. We
can assume that the widening of the lowfrequency
band characterizes the activation of perception pro
cesses, which has been reported to be stimulated with

estrogen [3941]. 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 2 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 2 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 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 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
frequency than in the state with a high progesterone
level and high 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 band are
reliable predictors of the activation response.
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CONCLUSIONS
An increased power suppression and a widened
individual lowfrequency 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 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 frequency EEG pattern.
Study of the activation level changes during the
ovarian hormonal cycle in women adds to our knowl
edge on the mechanisms of neuralvisceral 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.

1. Barry, R.J., Clarke, A.R., Johnstone, S.J., et al., EEG

differences between eyesclosed and eyesopen resting
conditions, Clin. Neurophysiol., 2007, vol. 118, p. 2765.
2. Venables, P.H. and Christie, M.J., Electrodermal activ
ity, in Techniques in Psychophysiology, Martin, I. and
Venables, P.H., Eds., Cambridge: University Press,
1980, p. 3.
3. Bai, X., Li, J., Zhou, L., and Li, X., Influence of the
menstrual cycle on nonlinear properties of heart rate
variability in young women, Am. J. Physiol. Heart Circ.
Physiol., 2009, vol. 297, no. 2, p. 765.
4. Blanchette, I. and Richards, A., Is emotional Stroop
interference linked to affective responses? Evidence
from skin conductance and facial electromyography,
Emotion, 2013, vol. 13, no. 1, p. 129.
5. Charlton, B.G., Noradrenergic innervation to the
adrenal cortex is responsible for control of basal gluco
corticoid secretion: a model, Med. Hypotheses, 1995,
vol. 44, no. 3, p. 214.
6. Huettel, S.A., Song, A.W., and McCarthy, G., Func
tional Magnetic Resonance Imaging, Massachusetts:
Sinauer, 2009, 2nd edition.
7. Jensen, O. and Mazaheri, A., Shaping functional archi
tecture by oscillatory alpha activity: gating by inhibi
tion, Front. Hum. Neurosci., 2010, vol. 4, no. 4, p. 186.
8. Tenke, C.E. and Kayser, J., Referencefree quantifica
tion of EEG spectra: combining current source density
(CSD) and frequency principal components analysis
Vol. 40

10.

11.

12.

13.

14.

15.

16.

REFERENCES

HUMAN PHYSIOLOGY

9.

No. 4

2014

17.

18.

19.

20.

21.

22.
23.

381

(fPCA), Clin. Neurophysiol., 2005, vol. 116, no. 12,

p. 2826.
Golubeva, E.A., Individualnye osobennosti pamyati
cheloveka: psikhofiziologicheskoe issledovanie (Individ
ual characteristics of human memory: a psychophysio
logical study), Moscow: Pedagogika, 1980.
Del Percio, C., Infarinato, F., Marzano, N., et al.,
Reactivity of alpha rhythms to eyes opening is lower in
athletes than nonathletes: a highresolution EEG
study, Int. J. Psychophysiol., 2011, vol. 82, no. 3, p. 240.
Bazanova, O.M. and Aftanas, L.I., Parameters of non
verbal creativity and individual frequency of maximum
activity peak in electroencephalogram, Funkts.
Diagn., 2006, no. 4, p. 43.
Hum, K.M., Manassis, K., and Lewis, M.D., Neural
mechanisms of emotion regulation in childhood anxi
ety, J. Child Psychol. Psychiatry, 2013, vol. 54, no. 5,
p. 552.
Dietrich, A., Althaus, M., Hartman, C.A., et al.,
Baroreflex sensitivity during rest and executive func
tioning in attentiondeficit/hyperactivity disorder: the
TRAILS study, Biol. Psychol., 2012, vol. 90, no. 3,
p. 249.
ChwalbiskaMoneta, J., Kruk, B., Nazar, K., et al.,
Early effects of shortterm endurance training on hor
monal responses to graded exercise, J. Physiol. Phar
macol., 2005, vol. 56, no. 1, p. 87.
Tenke, C.E., Kayser, J., Manna, C.G., et al., Current
source density measures of electroencephalographic
alpha predict antidepressant treatment response, Biol.
Psychiatry, 2011, vol. 70, no. 4, p. 388.
Wieck, A., GrassiOliveira, R., Prado, C.H., et al., Dif
ferential neuroendocrine and immune responses to
acute psychosocial stress in women with type 1 bipolar
disorder, Brain Behav. Immun., 2013. doi:ppi: S0889
1591(13)002390.10.1016/j.bbi.2013.07.005.
Muravleva, K.B., Kuzminova, O.I., Petrova, S.E.,
et al., Psychophysiological characteristics of women as
dependent on the phase of the ovarian hormonal cycle
and progesterone activity: part 1, Byull. Sib. Med.,
2013, vol. 12, no. 2, p. 247.
Kaplan, B.J., Whitsett, S.F., and Robinson, J.W., Men
strual cycle phase is a potential confound in psycho
physiology research, Psychophysiology, 1990, vol. 27,
no. 4, p. 445.
Baulieu, E.E., Neurosteroids: a novel function of the
brain, Psychoneuroendocrinology, 1998, vol. 23, no. 8,
p. 963.
Sofuoglu, M., Mouratidis, M., and Mooney, M.,
Progesterone improves cognitive performance and
attenuates smoking urges in abstinent smokers, Psycho
neuroendocrinology, 2011, vol. 36, no. 1, p. 123.
Conroy, S.K., McDonald, B.C., and Ahles, T.A., Che
motherapyinduced amenorrhea: a prospective study of
brain activation changes and neurocognitive correlates,
Brain Imaging Behav., 2013, vol. 7, no. 4, p. 491.
Walker, A.E., The Menstrual Cycle, London: Routledge,
1997.
Lu, Y., Bentley, G.R., Gann, P.H., et al., Salivary estra
diol and progesterone levels in conception and noncon
ception cycles in women: evaluation of a new assay for

382

24.

25.

26.

27.

28.

29.
30.

31.

32.

33.

BAZANOVA et al.
salivary estradiol, Fertil. Steril., 1999, vol. 71, no. 5,
p. 863.
Young, J. and Lester, D., Measuring anxiety on the
Lscher color test, Percept. Mot. Skills, 1994, vol. 3,
no. 2, p. 1106.
Khanin, Yu.L., Kratkoe rukovodstvo k primeneniyu shkaly
reaktivnoi i lichnostnoi trevozhnosti Ch.D. Spilbergera
(A Brief Guide to the Use of C.D. Spielbergers Scale of
State and Trait Anxieties), Leningrad: Len. Nauch.
Issl. Inst. Fiz. Kult., 1976.
Wijsman, J., Grundlehner, B., and Liu, H., Towards
mental stress detection using wearable physiological
sensors, Conf. Proc. IEEE Eng. Med. Biol. Soc., 2011,
p. 1798.
Makarenko, M.V., Lyzohub, V.S., and Iukhymenko, L.I.,
Heart rhythm in students with different individual and
typological characteristics of the higher nervous activity
during examination stress, Fiziol. Zh., 2003, vol. 49,
no. 1, p. 28.
Niizeki, K. and Saitoh, T., Incoherent oscillations of
respiratory sinus arrhythmia during acute mental stress
in humans, Am. J. Physiol. Heart. Circ. Physiol., 2012,
vol. 302, no. 1, p. 359.
Shepard, R.N. and Cooper, L.A., Mental Images and
Their Transformations, Cambridge, MA: MIT, 1982.
Einthoven, W., The discovery of the mechanism of the
electrocardiogram, in Nobel Lectures, Physiology or
Medicine, Amsterdam: Elsevier, 1965, p. 1922.
Bazanova, O.M., Variability and reproducibility of the
individual frequency of the maximum peak under dif
ferent experimental conditions, Zh. Vyssh. Nervn.
Deyat. im. I.P. Pavlova, 2010, vol. 60, no. 6, p. 767.
Hooper, G.S., Comparison of the distributions of clas
sical and adaptively aligned EEG power spectra, Int. J.
Psychophysiol., 2005, vol. 55, no. 2, p. 179.
Shmelkina, R., Some EEG findings caused by real and
imaginary stimuli in patients and healthy subjects, Appl.
Psychophysiol. Biofeedback, 1999, vol. 24, no. 2, p. 143.

34. Hamada, T., Koshino, Y., Fukui, J., and Tsubokawa, M.,
Reappearance and recovery of alpha rhythm after eye
opening, Rinsho Byori, 1990, vol. 38, no. 6, p. 711.
35. Koulen, P., Madry, C., Duncan, R.S., et al., Progester
one potentiates IP(3)mediated calcium signaling
through Akt/PKB, Cell Physiol. Biochem., 2008,
vol. 21, nos. 13, p. 161.
36. Freeland, K., Boxer, L.M., and Latchman, D.S., The
cyclic AMP response element in the Bcl2 promoter
confers inducibility by hypoxia in neuronal cells, Brain
Res. Mol. Brain Res., 2001, vol. 92, p. 98.
37. Klimesch, W., Sauseng, P., and Hanslmayr, S., EEG
alpha oscillations: the inhibitiontiming hypothesis,
Brain Res. Rev., 2007, vol. 53, p. 63.
38. Mazaheri, A. and Jensen, O., Posterior activity is not
phasereset by visual stimuli, Proc. Natl. Acad. Sci.
USA, 2006, vol. 103, no. 8, p. 2948.
39. Heimovics, S.A., Prior, N.H., Maddison, C.J., and
Soma, K.K., Rapid and widespread effects of 17
estradiol on intracellular signaling in the male songbird
brain: a seasonal comparison, Endocrinology, 2012,
vol. 153, no. 3, p. 1364.
40. Wibowo, E., Deurveilher, S., Wassersug, R.J., and
Semba, K., Estradiol treatment modulates spontaneous
sleep and recovery after sleep deprivation in castrated
male rats, Behav. Brain Res., 2012, vol. 226, no. 2,
p. 456.
41. Verrotti, A., Latini, G., Manco, R., et al., Influence of
sex hormones on brain excitability and epilepsy,
J. Endocrinol. Invest., 2007, vol. 30, no. 9, p. 797.
42. Bazanova, O.M., Gvozdev, A.V., Mursin, F.A., et al.,
EEGEMG dimensionality of the musical perfor
mance, Cogn. Proc., 2003, vol. 4, no. 3, p. 33.
43. Klimesch, W., Schimke, H., and Pfurtscheller, G.,
Alpha frequency, cognitive load and memory perfor
mance, Brain Topogr., 1993, vol. 5, no. 3, p. 241.
44. Klimesch, W., EEG alpha and theta oscillations reflect
cognitive and memory performance: a review and anal
ysis, Brain Res. Rev., 1999, vol. 29, p. 169.
Translated by V. Ushakov

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