ISSN 0362-1197, Human Physiology, 2018, Vol. 44, No. 1, pp. 1–6. © Pleiades Publishing, Inc., 2018. Original Russian Text © T.F. Shamaeva, M.V. Pronina, G.Yu. Polyakova, Y.I. Polyakov, V.M. Klimenko, 2018, published in Fiziologiya Cheloveka, 2018, Vol. 44, No. 1, pp. 5–11.
Electrophysiological Correlates of Major Depression Disorder with Anxious Distress in Patients of Different Age Groups T. F. Shamaevaa, *, M. V. Proninab, G. Yu. Polyakovac, Y. I. Polyakovb, and V. M. Klimenkoa aInstitute
of Experimental Medicine, St. Petersburg, 197376 Russia Institute of the Human Brain, St. Petersburg, 197376 Russia c Mechnikov Northwestern State Medical University, St. Petersburg, 191144 Russia *e-mail:
[email protected] bBechtereva
Received December 8, 2016
Abstract—The electrophysiological correlates of major depression disorder with anxious distress in patients of different age groups have been investigated. The spectral characteristics of 19-channel background EEG were analyzed and the power spectra recorded with the eyes closed vs. eyes open in 64 patients with anxiety– depressive disorder and in 194 healthy subjects were compared. The subjects were divided into the two age groups: 18–39 and 40–76 years old. The spectral parameters were calculated for 5 main EEG frequency bands: θ (4–8 Hz), α (8–12 Hz), β1 (12–20 Hz), β2 (20–30 Hz), and γ (30–40 Hz). The most statistically significant differences between the groups were found in the α, β, and γ bands. Lower values of spectral power of the α rhythm in occipital areas and the higher values of spectral power of the β and γ rhythms in the frontocentral region were recorded in the group of 18-to-39-year-old patients with the eyes closed. Higher values of spectral power of the β rhythm in the fronto-central region and in the left temporal lobe were recorded in the group of 40-to-76-year-old patients with both the eyes closed and the eyes open. The higher β-activity in the fronto-central regions in both groups of patients may be caused by increased excitability of the cerebral cortex and decreased activity of inhibitory processes. Increased activation of the left temporal lobe in older subjects is probably associated with the severity of anxiety symptoms and may be a distinctive marker of mixed anxiety and depressive disorder. The lower values of α-power revealed only in the group of younger subjects are probably associated with age-related reorganization of EEG in older subjects. Keywords: major depression disorder with anxious distress, electroencephalography, age-related features, spectral analysis DOI: 10.1134/S0362119718010152
In recent years, numerous studies and large numbers of visits to clinics have shown the rapid spread of affective disorders among millions of people. Depressive disorder is currently one of the most common diseases. According to the prognosis of the World Health Organization (WHO), in 2020 depressive episodes will take second place in the world among all diseases, next to ischemic heart disease [1]. However, the problem of diagnosing major depressive disorder, in spite of its long-term and thorough investigation, is still poorly studied and extremely topical. The psychometric scales and relatively subjective clinical interviews are the basic methods for the detection of depressive disorder and assessment of its severity. The absence of objective instrumental diagnostics results in erroneous interpretation of affective pathology.
rent functional state of different areas of the cerebral cortex during quiet wakefulness. According to the published scientific data, a great number of electrophysiological correlates of depressive disorders have been revealed so far. One of the most frequent alterations in the spectral characteristics of EEG in depressive states is frontal α-rhythm asymmetry. Since α-rhythm power is inversely proportional to activation of the respective brain region, Davidson et al. assert that frontal α-asymmetry directly reflects the difference in activation between the right and left hemispheres [2, 3]. The study of electrical activity of the brain in patients with depressive disorders compared to health people showed the high values of α-rhythm in the frontal leads of the left hemisphere compared to the right one; at the same time, there was no significant difference between the hemispheres in central and occipital brain regions [4–6]. Further investigation of depressive disorders showed substantial reorganization of the power of
One of the promising and important methods for the study of neurophysiological mechanisms of pathogenesis of depressive disorders is electroencephalography (EEG). EEG makes it possible to assess the cur1
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other spectral bands over nearly the entire cortex. A statistically significant increase in β-rhythm power is reported mainly in the frontal cortical areas by some authors [7, 8] and in the occipital areas by other authors [9, 10]. In addition, the high values of γ-rhythm power (30−40 Hz) were observed in the frontal and temporal cortical areas [11]. Pollok and Schneider draw a conclusion on the higher power of α- and β-rhythms during depressive disorders compared to the control group [12]. Hughes and John in their review conclude that the patients suffering from depressive disorders have the higher values of α- and θ-rhythm power, as well as the marked asymmetry in the frontal cortical areas, most often in the event of recurrent depressions. The low power of α-activity and the high power of β-rhythm are observed for bipolar disorder [13]. The described studies were devoted mainly to the search of neurophysiological features common to all clinical variants of depressions. However, there are almost no data on neurophysiological differences between depressive syndromes with diverse psychopathology, probably due to the diversity and inconsistency of findings. Search range reduction and identification of neurophysiological correlates for each variant of depressive syndrome, according to its psychopathological pattern, will give more accurate and clinically significant results. Mixed anxiety and depressive disorder is one of the most frequent (and the major) syndrome in the entire group of affective disorders [14]. According to the United States National Comorbidity Survey, depression is detected in almost 60% of patients with anxiety disorders [15]. The mixed anxiety and depressive disorder is characterized by pronounced manifestations of anxiety, inner restlessness, low mood, diurnal mood variation, sleep–wake disorders, low cognitive performance (memory and attention impairment), and fears. The somatic (autonomic) symptoms include palpitation, muscle spasms, tremor, muscle pains, loss of appetite, weight loss, constipation, nausea, and headache. Due to the high variability of EEG patterns in patients with depression, the aim of this study was to identify the neurophysiological correlates of the mixed anxiety and depressive disorder in patients of different age groups. METHODS The research was carried out pursuant to the modern commonly accepted principles of biomedical ethics. The studies were performed in 64 patients at the age of 18 to 76 years (46 women and 18 men): 24 patients with the current episode of depression in bipolar affective disorder (F31.3) and 40 patients with the current episode of depression in recurrent depressive disorder (F33.0, F33.1, F33.2). The clinically verified diagnosis was made in accordance with ICD-10. Mixed anxiety and depressive disorder was identified
in all patients by the syndromal symptom, according to the classification of Nuller and Mikhalenko [16]. Psychotropic drugs were administered to all patients at the moment of examination. 42 patients took antidepressants from the group of serotonin noradrenaline reuptake inhibitors (Rexetin, Cymbalta, Venlafaxine) and preparations from the group of anxiolytics (phenazepam); 22 patients took only antidepressants (serotonin noradrenaline reuptake inhibitors). The intensity of anxiety and depressive symptoms was determined by using the clinical-psychopathological technique and psychometric scales. The clinical-psychopathological technique was used to verify the diagnosis in accordance with ICD-10. The severity of depression was assessed by the standardized and objective Montgomery–Asberg Depression Rating Scale (Montgomery and Asberg, 1979). The intensity of depression was determined by the total score. In the examined group, the level of disorder corresponded to minor depressive episode in 12 patients, moderate depressive episode in 43 patients, and major depressive episode in 9 patients. The intensity of anxiety in the structure of psychopathological syndrome was assessed by the Hamilton Anxiety Rating Scale (Hamilton, 1960). According to the results of examination by this scale, 40 patients had a total score of 18 to 24, demonstrating the moderate intensity of the anxiety component; severe anxiety was detected in 24 patients (more than 25 points). The reference HBI Database was used as a control group. The main criteria for identifying apparently healthy subjects in the database were as follows: the prenatal period without pathology, the absence of neurological and psychic disorders, traumatic brain injuries, convulsive and paroxysmal activity in past history; at the moment of examination, all subjects gave their voluntary consent and did not take medicines [17]. The anxiety and depressive symptoms were revealed in all patients and, according to the published data, the age-related changes in EEG organization were revealed during normal aging [18]; hence, in this research all patients were combined into a single group by the syndromal symptom. The patients were divided into two age groups for more correct comparison with the normative database. The first group of patients included 29 subjects at the age of 18–39 years (6 men, 23 women; mean age, 29.4 ± 1.9 years); the second group included 35 subjects at the age of 40 to 76 years (12 men, 23 women; mean age, 55.7 ± 3 years). The group of apparently healthy subjects included 96 subjects at the age of 18–39 years (49 men, 47 women; mean age, 28.8 ± 1.3 years) and 98 subjects at the age of 40 to 75 years (54 men, 44 women; mean age, 53.9 ± 1.7 years). Neurophysiological examination included the multichannel recording of background EEG during HUMAN PHYSIOLOGY
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quiet wakefulness with the eyes open and closed (3 min per sample). EEG was recorded with a Mitsar hardware and software complex (Mitsar, St. Petersburg, Russia), a 19-channel electrode cap from ElectroCap (ElectroCap, Eaton, Ohio, United States), and the Win EEG computer software (created by V.A. Ponomarev). Bioelectrical brain activity was recorded according to the International 10–20 System of electrode placement in the following leads: Fp1; Fp2; F7; F3; Fz; F4; F8; T3; C3; Cz; T4; T5; P3; Pz; P4; T6; O1; O2. Ear-clip electrodes A1 and A2 were used as reference electrodes; the ground electrode was placed in the Fpz lead. Electrode resistance did not exceed 5 kΩ. The pass bands were 0.53 Hz and 30 Hz; the band elimination filter was 45–55 Hz; the EEG sampling rate was 250 Hz. The oculogram and myogram were corrected by independent component analysis (ICA) [19]. The spectral analysis of the results was performed by the fast Fourier transform algorithm in the range of 4–40 Hz, followed by the mapping of EEG spectral power. The quantitative estimates of EEG spectral power were made in the narrow frequency bands: θ (4–8 Hz), α (8–12 Hz), β1 (12–20 Hz), β2 (20– 30 Hz), and γ (30–40 Hz). The spectral analysis of EEG was statistically processed using the Statistica data processing software package. The confidence intervals at a significance level (0.99 and 0.999) were calculated for EEG power logarithms in each frequency band of all 19 channels for the states with open and closed eyes in each of the age groups separately. The statistical analysis of the parameters under study was performed using the Student’s test (t) for independent samples with the Bonferroni connection. Cohen’s d effect size was also calculated for qualitative assessment of the detection of differences in EEG spectral power between the groups of patients (the effect size was at a level of d > 0.8) [20]. RESULTS There were significant differences between the group of patients and the group of apparently healthy subjects at the age from 18 to 39 in EEG records with the eyes closed detected as the lower values of α-rhythm power in the parietal (P3, Pz, P4) and occipital (O1, O2) leads: F(1,125) = 15.057, p < 0.0001, d (Cohen) = 0.83. In addition, there were significantly higher power values in the β2 frequency band in the frontal leads (F7, Fz, F8): F(1,125) = 14.812, p < 0.0001, d (Cohen) = 0.82, and the higher power values in the γ-band in the frontal (mainly on the right) and central leads (F7, Fz, F4, F8, Cz): F(1,125) = 16.929, p < 0.00007, d (Cohen) = 0.88. There were no significant differences in EEG records with the eyes open. The 40- to 76-year-old patients with the anxiety and depressive disorder were shown to have significantly higher (compared to the normative base) power HUMAN PHYSIOLOGY
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values in the fronto-central cortical areas and in the left temporal area (F3, Fz, Cz, T3) in the frequency bands β1: F (1,133) = 4.181, p < 0.00005, d (Cohen) = 0.83 and β2: F (1,133) = 4.803, p < 0.000004, d (Cohen) = 0.95 for EEG records with the eyes closed. With the eyes open, the significantly higher power values were revealed in the β2-band in the lead Cz: F (1,133) = 4.365, p < 0.00002, d (Cohen) = 0.86, and in the β1-band in the temporal leads (T3, T4): F (1,133) = 4.289, p < 0.00003, d (Cohen) = 0.85. Figure 1 shows the differences in logarithmic values of EEG spectral power between the groups of patients of different age and the reference database for the “eyes open” and “eyes closed” EEG records. Gradations of gray indicate the statistical significance of differences. The intra-group analysis of spectral power demonstrates the asymmetry in some frequency bands. Table 1 shows the differences between the medians for the difference in logarithmic values of spectral power in the frontal and temporal leads for the groups of patients and apparently healthy subjects in two age groups. The statistical significance of the results was tested by the Student’s t test for independent samples. DISCUSSION Despite the great number of neurophysiological studies in the field of affective disorders, the vast diversity of electroencephalographic manifestations of depressive states can be associated with the clinical polymorphism of depression and the absence of a uniform estimate for pathological state. One should take into account not only the severity, manifestations and structure of depressive disorder gravitating to the poles of excitation (anxiety depression) or inhibition (melancholic depression) but also the age-related peculiarities of EEG reorganization. The results demonstrate specific deviations of EEG spectral power in patients with the anxiety and depressive disorder from different age groups. The maximum changes in bioelectrical brain activity were revealed for EEG records with the eyes closed in both groups. The 19- to 39-year-old patients with the eyes closed were shown to have significantly lower values of α-rhythm power in the parieto-occipital cortical areas and higher values of high-frequency activity in the fronto-central region; in the 40- to 76-year-old patients, significant differences were observed only in the fronto-central and temporal regions. These changes are associated with the processes of cortical hyperexcitability and the decreased activity of inhibitory processes [8, 10, 14]. According to the published data, the age-related changes in EEG organization were revealed during normal ageing as the lower values of α-rhythm power in the parietal-occipital leads [21,
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Eyes closed
α
Eyes open θ
θ 0.00001 0.00005 0.0001 0.0005 0.001 0.005 0.010 0.025 0.05 –0.05 –0.025 –0.010 –0.005 –0.001 –0.0005 –0.0001 –0.00005 –0.00001
α
Eyes closed θ
0.00001 0.00005 0.0001 0.0005 0.001 0.005 0.010 0.025 0.05
0.00001 0.00005 0.0001 0.0005 0.001 0.005 0.010 0.025 0.05
0.00001 0.00005 0.0001 0.0005 0.001 0.005 0.010 0.025 0.05 –0.05 –0.025 –0.010 –0.005 –0.001 –0.0005 –0.0001 –0.00005 –0.00001
Eyes open θ
α
–0.05 –0.025 –0.010 –0.005 –0.001 –0.0005 –0.0001 –0.00005 –0.00001
α
β1
β1
β1
β1
β2
β2
β2
β2
γ
γ
γ
γ
Age from 18 to 39 years
–0.05 –0.025 –0.010 –0.005 –0.001 –0.0005 –0.0001 –0.00005 –0.00001
Age from 40 to 76 years
Fig. 1. The intergroup differences between the logarithmic values of EEG spectral power in each frequency band of all 19 channels with the eyes closed and open.
22]. Accordingly, the older patients showed no reliable differences in α-band against EEG reorganization. In particular, the older patients were shown to have the left-sided asymmetry in α-, β1-, β2-bands in the temporal lobe with the eyes closed; in addition, significant differences were revealed in α-band in the frontal areas between the group of apparently healthy subjects and the group of patients with the anxiety and depressive disorder at the age of 40 to 76. The younger patients were not shown to have any statistically significant differences. Since α-rhythm power is inversely proportional to activation of the respective brain regions, Rotenberg asserts that the frontal asymmetry directly reflects the difference in activation between the right and left hemispheres [3]. Cortical activation is manifested as EEG desynchronization, i.e., in the high-frequency band. Accordingly, the higher values of α-rhythm power in the frontal leads of the right hemisphere correspond to the lower activation in this area. The majority of studies searching for EEG markers of depressive states demonstrate a relationship between hyperactivation of the right fronto-temporal region and depression [23, 24]. At the same time, there are many works indicating the high power values of high-frequency activity in the left fronto-temporal region [25, 26]. One of the causes of ambiguity of the data obtained may be the heterogeneity of depressive disorder and the influence of anxiety disorder.
The older patients diagnosed in the framework of this study complained of the feelings of anxiety, uneasiness, fear, internal excitement, the higher level of agitation, sleep disorders, as well as autonomic disorders, such as dysfunction of some organs, rather than of depressive state of mind. The prevalence of somatic complaints and the high share of anxiety components are the peculiar features of late-life depression, rather than low mood [27]. The study by Heller et al. has shown an increase in activity of the left cerebral hemisphere during anxious or panic excitation [28]. Thus, it can be supposed that that the increase in the spectral characteristics of fast-wave activity of the left temporal lobe in older patients demonstrates the prevalence of a marked anxiety component. In addition, the intensified activation of temporal cortical areas closely related to emotiogenic limbic structures revealed in the group of 40- to 76-year-old patients, according to the published data, can represent the degree of intensity of affective disorder [29]. The examination of 40- to 76-year-old patients did not show the normal asymmetry of α-activity in the frontal areas, probably due to the therapy administered. The high values of high-frequency activity in the fronto-central regions are associated with the marked anxiety in patients and probably mask the asymmetry of α-rhythm power [30]. It should be noted that in this research we divided patients into groups without taking into consideration the influence of gender differences and the pathogenesis of depressive disorder. According to the published HUMAN PHYSIOLOGY
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Table 1. The intergroup differences between the medians of difference of the logarithmic values of spectral power in the fronto-temporal leads EEG frequency bands and leads under study
Median value of the difference of logarithms of spectral power with the eyes closed
age
18 to 39 years
group α
β1
β2
γ
AS
40 to 76 years AH
AS
AH
F4–F3
0.0178
0.0313
0.0076*
0.0532*
F8–F7
0.0329
0.0568
0.0165
0.0298
T4–T3
0.0257
0.0180
–0.0454*
0.0351*
F4–F3
0.0334
0.0335
–0.0003
0.0308
F8–F7
0.0473
0.0331
–0.0027
0.0523
T4–T3
0.0248
0.0016
–0.0569*
0.0382*
F4–F3
0.0298
0.0285
–0.0232
0.0239
F8–F7
0.0591
0.0403
–0.0239
0.0497
T4–T3
0.0361
0.0004
–0.0931*
0.0307*
F4–F3
0.0425
0.0125
–0.0466
F8–F7
0.1096
0.0298
–0.0452
0.0455
T4–T3
0.0270
–0.0188
–0.0872
0.0338
–0.017
* Significant difference (p < 0.05); AS is the group of patients with mixed anxiety and depressive disorder; AH is the group of apparently healthy subjects; α, β1, β2, γ are the EEG frequency bands.
data, these factors can affect the results of research. It has been shown that the level of activation of the central nervous system in women is higher compared to men, which is reflected in amplification of the indices and average spectra of the lower and upper β-rhythms [31]. Unipolar depression is also characterized by the lower values of EEG activity in the left frontal cortex, while the higher values of EEG activity in this region are typical of bipolar disorder [32]. The study of quantitative characteristics of the background EEG in the patients with mixed anxiety and depressive disorder receiving drug therapy is also an important factor of research. It is known that the pharmacological tests with administration of phenazepam have shown the higher power values in the β2-band on EEG, as well as the higher coherence values in the β2- and γ-bands, mainly in the frontal and fronto-temporal regions [33, 34]. Accordingly, the pharmacological therapy administered to the patients in our research could influence the results obtained. Thus, further studies should be carried out with due consideration of the gender factor, the subtype of depression by the main syndrome, etiological basis, as well as resistance to antidepressant treatment and influence of drug therapy. CONCLUSIONS The results of this study confirm the presence of specific deviations of the functional state of the cereHUMAN PHYSIOLOGY
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bral cortex from normative data in the patients with mixed anxiety and depressive disorder from different age groups. The changes in α-rhythm power emphasize age-related characteristics of EEG reorganization in patients of the older age group, while the higher values of β-rhythm power in the fronto-central regions in both groups under study are indicative of the processes of cortical hyperexcitability. Enhanced activation of the left temporal lobe in older patients probably reflects the degree of manifestation of the anxiety component in depressive disorder. The impaired brain function revealed in the patients with mixed anxiety and depressive disorder indicates that it is necessary to take into account not only the severity of depressive state but also the concomitant syndromal symptoms, as well as the age-related features of spectral characteristics of the brain and the influence of drug therapy. ACKNOWLEDGMENTS This study was supported by the Russian Foundation for the Humanities (project no. 14-06-00973a). REFERENCES 1. Lopez, A. and Murray, C., The global burden of disease, 1990–2020, Nat. Med., 1998, vol. 4, p. 1241. 2. Davidson, R.J., EEG measures of cerebral asymmetry: conceptual and methodological issues, Int. J. Neurosci., 1988, vol. 39, nos. 1–2, p. 71.
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