Human Physiology, Vol. 30, No. 4, 2004, pp. 392–396. Translated from Fiziologiya Cheloveka, Vol. 30, No. 4, 2004, pp. 19–24. Original Russian Text Copyright © 2004 by Nikishena, Ponomarev, Grin’-Yatsenko, Kropotov.

Mapping of Changes in EEG Spectrum Power during a Session of Biofeedback Training of the b1 Rhythm I. S. Nikishena, V. A. Ponomarev, V. A. Grin’-Yatsenko, and Yu. D. Kropotov Institute of the Human Brain, Russian Academy of Sciences, St. Petersburg, 197022 Russia Received March 17, 2003

Abstract—Changes in EEG spectrum power from 19 electrode sites were studied in 19 children with attention disorders during one session of EEG–biofeedback (EEG–BFB). EEG–BFB was aimed at increasing the relative power of the β1 rhythm (15–18 Hz) in sites Fz–C3 with a bipolar electrode assembly. Comparison of the EEG spectrum powers at relaxation versus training periods in one BFB session revealed significant changes in the left parasagittal frontoparietal area (F3, Fz, C3, C4, P3).

Attention deficit hyperactivity disorder (ADHD) is considered to be the most frequent chronic behavioral disorder in children and adolescents [1]. The ADHD incidence among children of school age ranges from 3 to 20% according to different estimates [2–4]. Recent studies have shown that the EEG of healthy subjects differs from the EEG of children with attention deficit [5–7]. In children with ADHD, spectrum power is characterized by an increase in slow-wave activity in the range of θ waves, predominantly in frontal areas [5, 8−12], and/or by a decrease in activity in the range of 12–21 Hz [8, 13]. Particularly, a generalized and/or local increase in spectrum power of the θ activity in the frontal and central areas has been observed in 76.2% of children with ADHD or attention deficit disorder (ADD) without hyperactivity, and a drop in spectrum power of β1 rhythms has been revealed in 13.1% of cases [5]. According to the data of positron emission tomography, magnetic resonance imaging, and cerebral blood flow studies, biochemical and anatomical defects of cortical and subcortical regions of the brain may be assumed for children with ADHD or ADD. Dysfunction and/or structural changes in the frontostriatal system have been reported for such children [3, 14–17]. Presumably, ADHD signs such as attention deficit, hyperactivity, and impulsiveness are associated with insufficient activation of the frontal cortex in combination with dysfunction of the basal ganglia and midbrain structures. Neurotherapy, or biofeedback (BFB), is one of the methods of ADHD therapy [2]. Neurotherapy protocols are aimed at suppressing the slow activity in the θ band (4–7 Hz) and increasing the rapid activity in the β1 band (15–18 Hz). The effectiveness of neurotherapy in ADHD has been demonstrated in a number of works [18, 19]. Studies of the correlated changes in brain activity commonly report an improvement of the state according to clinical signs and psychological scales. Only a few

studies have focused on changes in neurophysiological correlates during neurotherapy. Mainly, the changes in the EEG from one channel have been analyzed in the course of a BFB session. Lubar et al. [11] showed that BFB training with respect to the ratio between the powers of θ and β1 activities significantly decreased this ratio as compared with that before a training course. The increase was observed with all EEG channels over the entire head surface, although BFB training employed only one bipolar lead at the median line. The goal of our work was to study the topography of changes in EEG spectrum power during a session of BFB training with respect to relative β1 rhythms. We formulated the following tasks: (1) to record the EEG from 19 standard derivations during an EEG–BFB session, (2) to analyze the EEG spectrum power in two states (relaxation, training), and (3) to estimate the ratio of spectrum powers (β1/α and β1/θ) in these states. METHODS A group of 22 children (20 boys and 2 girls aged 9−14 years) with signs of ADHD participated in the study. ADHD was diagnosed on the basis of interviews with parents, psychological tests, neurological examination by DSM-IV criteria [1], and evoked potentials in the two-stimuli Go/No-Go paradigm [18]. The administration of psychostimulants and antidepressants was not performed during BFB sessions and testing in all patients. Psychological testing included the test of variables of attention (TOVA) [20]. The TOVA has been developed as a test for continuous activity, is based on presentation of significant (requiring a response, Go) and insignificant (requiring no response, No-Go) visual stimuli, and reports the state of the attention in relation to the standard level. The TOVA data allow estimation of the attention deficit (omission errors, i.e., missed tar-

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get), impulsivity (commission errors, i.e., wrong response), response time, and variance of the response time. All participants underwent 15–20 sessions of β1 training. To eliminate high anxiety and achieve muscle relaxation, the first five sessions each included α training (5 min) along with BFB training with respect to β1 rhythms. Starting from the sixth session, α training was withdrawn, and a session of β1 training was followed by a 5-min session aimed at enhancing sensorimotor rhythm. Sessions of β1 training were carried out according to a protocol developed in the Laboratory of Neurobiology of Action Programming. The protocol implied an increase in the relative power of β1 rhythms (15– 18 Hz) of the left hemisphere in children of all age groups [18]. The relative β1 power was calculated as the ratio of the absolute β1 power to the sum of the absolute powers of the θ, α, sensorimotor, and β2 rhythms. Electrodes involved in β1 training were attached above the frontal (Fz) and sensorimotor (C3) zones of the left hemisphere in a bipolar assembly. A patient was seated in a comfortable armchair 0.7–1.0 m away from a computer screen. A feedback signal was presented on the screen as a blue column with the amplitude depending on the ratio between the power of β1 rhythms and the total powers of all other oscillations. Feedback signals were calculated for 1-s periods, and the column presented on the screen was updated every 250 ms. The blue column was presented against a gray background, which was divided by a horizontal threshold line into upper (light gray) and lower (dark gray) parts. The patient was instructed to retain the column on the light gray background as long as possible. For this, the patient was asked to sit motionlessly in a comfortable posture, relax, concentrate his or her attention on a spot close to the column, and watch the changes in its amplitude. The task of the subject was to memorize his or her internal state when the column was on the light gray background (i.e., it was higher than the threshold) and to reproduce this state. The threshold was estimated during a session as the mean ratio between the β1rhythm power and the total power of all other oscillations in a 150-s EEG recorded before β1 training and was usually 0.03–0.05. The patient was supervised by a researcher throughout a session. During relaxation periods, the patient’s EEG was presented in the upper one-third of the screen and the current training plot was shown at the bottom. The patient was recommended to relaxation and keep his or her eyes open without watching the plot. A session of β1 training included EEG recording for 150 s before training and three 4-min periods of β1 training, which were separated by 1-min intervals of relaxation. Usually, patients successfully performed the task after 8–10 training sessions. A BFB session was considHUMAN PHYSIOLOGY

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ered to be successful when the patient increased the target ratio over the background value in all training periods. The successfulness of training was estimated after each session by the time plot of the ratio of the β1-spectrum power to the total power of all other oscillations. A continuous multichannel EEG was recorded in parallel with BFB training. In three previous sessions, all children showed a stable increase in the ratio between the powers of the β1 rhythm and all other oscillations during training as compared with the ratio established with a background EEG. The EEG was recorded by means of a Mitsar 201 21-channel digital encephalograph (Mitsar, St. Petersburg) from 19 AgCl cap electrodes fixed on the head surface with a Ten20 conductive paste. The electrodes were located according to the 10–20 international system at points Fp1, Fp2, F7, F3, Fz, F4, F8, T3, C3, Cz, C4, T4, T5, P3, Pz, P4, T6, O1, and O2. All scalp recordings were referenced to linked earlobes, and the grounding electrode was in the frontal area (Fpz). The electrode impedance did not exceed 10 kΩ. The parameters of high-cut- and low-cut-frequency filters were 1.5 Hz (0.1 s) and 30 Hz, respectively. The digitization rate was 250 Hz. The EEG study was carried out during one of the 10th to 13th sessions of BFB training. Preliminarily, the EEG was analyzed visually. EEGs with extended movement or frontal muscular tension artifacts were excluded from the analysis. Grand averaged power spectra were estimated separately for three sequential periods of β1 training and three periods of relaxation (one background EEG record before training and two records between training periods). The relative powers of the θ (4–7.5 Hz), α (8−12 Hz), sensorimotor (12–15 Hz), β1 (15–18 Hz), and β2 (18–25 Hz) rhythms and the ratio between the relative β1 power and the relative powers of the α and θ rhythms were compared for relaxation and training with the use of the nonparametric sign test. RESULTS Three EEG records (one girl’s and two boys’) were excluded from the analysis because of numerous physiological artifacts (muscle contractions in the frontal, temporal, and occipital regions). The TOVA was performed to estimate the attention and impulsivity of the children before and after the EEG–BFB training. According to the TOVA results, 16 out of the 19 children had lower parameters of attention: the number of Go-stimulus omission errors was one or two standard deviations below the average in five children and three standard deviations below the average in ten children. A decrease in impulsivity control was detected in 15 children (the number of wrong responses was one or two standard deviations below the average in 13 subjects and more than three standard deviations below the average in 2 subjects). The reaction time was increased in six children; in three of

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Fig. 1. Dynamics of the ratio between the β1-rhythm power and the total power of other EEG spectrum bands during periods of (1) relaxation and (2) β1 training during an EEG– BFB session. Abscissa, time, s; ordinate, ratio between the β1-rhythm power and the power of the other EEG spectrum bands, arbitrary units.

these, the increase exceeded two standard deviations in both parts of the test; in the other three, it exceeded one standard deviation in the first part of the test. Comparison of the TOVA data obtained before and after BFB training in the 19 children showed the following results. The number of commission errors in response to No-Go stimuli significantly decreased after EEG–BFB training in both parts of the test (Z = 2.25, P < 0.024, and Z = 2.425, P < 0.015, for the first and second parts, respectively). The reaction time decreased in the second part of the test (Z = 2.25, P < 0.024). The number of correct responses to Go stimuli increased in both parts of the test, but the increase was nonsignificant (P < 0.05). Spectral analysis of the EEG. A time plot of the ratio between the power of the β1 rhythm and the relaxation of the EEG spectrum was recorded in the C3–Fz lead during a BFB session. For easier visual examination, the time plot was smoothed by averaging the values in a sliding window of a width of 100 measurements (25 s); this allowed rapid assessment of the efficiency of the BFB session (Fig. 1). As seen from the figure, the trained ratio increased as compared to the background during training and decreased to the background level or below it during relaxation. The grand averaged power spectra recorded at relaxation and during training are presented in Fig. 2. EEGs recorded during β1 training were characterized by an increase in the relative power of the β1 rhythm in elec-

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–1 Fig. 2. Average plots of EEG power spectra in children with ADHD in the periods of relaxation and BFB training (monopolar montage). The differences are shaded. Abscissa, frequency, Hz; ordinate, logarithm of spectrum power amplitude (lg(P)).

trode site F4 (Z = 1.96, P < 0.05) as compared to EEGs recorded at relaxation. It should be noted that EEG power spectra varied in frequency distribution among the children examined. To eliminate the interindividual variation of spectra, we calculated the ratios of the β1-rhythm power during training to the α-rhythm power (β1 rhythm/α rhythm) and to the θ-rhythm power (β1 rhythm/θ rhythm). No significant changes were observed for the β1-rhythm/θ-rhythm ratio. During β1 training, an increase in the β1-rhythm/αrhythm ratio was recorded in sites F3 (Z = 2.33, P = 0.019), C3 (Z = 2.27, P = 0.023), P3 (Z = 2.27, P = 0.023), Fz (Z = 2.08, P = 0.037), and C4 (Z = 2.004, P = 0.04). Figure 3 shows the topograms of the β1-rhythm/α-rhythm ratio during relaxation (Fig. 3, 1) HUMAN PHYSIOLOGY

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Fig. 3. Topography of changes in the β1-rhythm/α-rhythm power ratio in the periods of (1) relaxation and (2) training during a BFB session. The scale shows the β1-rhythm/α-rhythm power ratio in arbitrary units.

and during training (Fig. 3, 2) as averaged over the entire group. DISCUSSION The main aim of this work was to study the brain bioelectrical activity in the EEG band during a session of neurotherapy. In most studies of the changes associated with BFB training, the analysis includes only the recording used to obtain a feedback signal, i.e., a recording from one EEG electrode. In our study, the EEG was recorded from 19 scalp electrodes. This method makes it possible to estimate profoundly the EEG changes taking place during a BFB session. In children with ADHD subjected to neurotherapy, changes in EEG spectrum powers were observed during training as compared to periods of relaxation. The changes were recorded in the α and β1 bands. Since significant differences were obtained for the β1-rhythm/αrhythm ratio, we might suppose that the increase in the power of the β1 rhythm as compared to other frequency bands during the BFB session was due to two processes: first, enhancement of β1 rhythm power and, second, a decrease in low-frequency α rhythm power. Probably, the therapeutic influence of BFB results in two processes, activation of the β1 rhythm and inhibition of the α rhythm. The contributions of these two processes differ and depend on the location of an electrode. Changes in the β1 rhythm were observed in the frontal and central areas, whereas the power of the α rhythm decreased predominantly in the posterior regions. Changes in the EEG α band during the performance of different tasks are considered to be mostly or even exclusively related to nonspecific factors: attention and wakefulness levels and emotions. In particular, inhibition of α activity is of functional importance when the corresponding cortical areas are involved in a certain activity [21]. This assumption agrees with the view that the α rhythm testifies to an “idling” of the brain and that inhibition of the α rhythm is an essential prerequisite to HUMAN PHYSIOLOGY

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efficient processing of information. Thus, during task performance demanding a high level of attention, the activity of various cortical areas increases, which is seen in a decrease in α-rhythm power in these regions. Most researchers consider β activity to reflect the cognitive processes and concentration of attention. The functional role of the β rhythm is generally associated with the processing of stimuli in the frontal cortex; however, studies of the β rhythm are still at the stage of description. An increase in the β rhythm takes place upon presentation of significant stimuli [22, 23]. In general, it is possible to suppose that changes in β activity are to a substantial extent a dynamic characteristic and that its increase is short-term. In fact, the only work focusing on the dynamics of EEG spectrum power during BFB therapy was carried out by Lubar et al. [11]. A significant change in the power of the trained parameter was observed after 35– 40 sessions of neurotherapy. In our study, the changes were only local as compared with the above work. The difference from the results of Lubar et al. [11] is likely to be explained by the fact that we recorded the EEG only during one session of BFB training rather than after the completion of a BFB course. However, it is noteworthy that the changes in power were recorded not only in the electrode sites used to generate the feedback signal (Fz–C3) but also in other brain areas. Our results allow us to conclude that the changes during BFB therapy are not strongly local nor restricted to particular regions of the brain. Analysis of the EEG spectrum power revealed substantial changes in the frontal, left parietal, and sensorimotor cortex. It is these areas that are considered to be a neuroanatomical substratum of attention deficit and hyperactivity [3, 15, 16]. Our findings suggest that EEG–BFB has an effect on both specific and nonspecific mechanisms of attention.

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CONCLUSIONS During EEG–BFB, children with ADHD showed an increase in the β1-rhythm/α-rhythm power ratio in electrode sites F3, Fz, C3, P3, and C4 during β1 training. The maximum decrease in α-rhythm power was noted in the posterior regions of the brain, while changes in the β1 rhythm were most considerable in the frontal and central brain regions. ACKNOWLEDGMENTS This work was supported by the Russian Foundation for Basic Research (project no. 00-15-97893) and the Russian Humanitarian Scientific Foundation (project no. 01-06-00160i).

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