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Appl Psychophysiol (2015) 40:17–24 DOI 10.1007/s10484-015-9269-x

Effects of Neurofeedback on Adult Patients with Psychiatric Disorders in a Naturalistic Setting

Eun-Jin Cheon • Bon-Hoon Koo • Wan-Seok Seo • Jun-Yeob Lee • Joong-Hyeon Choi • Shin-Ho Song

Published online: 5 March 2015 Ó Springer Science+Business Media New York 2015

Abstract Few well-controlled studies have considered rating scale also showed significant differences in depres- neurofeedback treatment in adult psychiatric patients. In sive symptoms, anxiety, and inattention (\.001). This is a this regard, the present study investigates the characteris- naturalistic study in a clinical setting, and has several tics and effects of neurofeedback on adult psychiatric limitations, including the absence of a control group and a patients in a naturalistic setting. A total of 77 adult patients heterogenous sample. Despite these limitations, the study with psychiatric disorders participated in this study. demonstrates the potential of neurofeedback as an effective Demographic data and neurofeedback states were retro- complimentary treatment for adult patients with psychiatric spectively analyzed, and the effects of neurofeedback were disorders. evaluated using clinical global impression (CGI) and sub- jective self-rating scales. Depressive disorders were the Keywords Neurofeedback Á Adult psychiatric patient Á most common psychiatric disorders (19; 24.7 %), followed Depression Á Anxiety by anxiety disorders (18; 23.4 %). A total of 69 patients (89.6 %) took , and the average frequency of neurofeedback was 17.39 ± 16.64. Neurofeedback was Introduction applied to a total of 39 patients (50.6 %) more than 10 times, and 48 patients (62.3 %) received both b/SMR and There are two conventional treatment modalities in psy- a/h training. The discontinuation rate was 33.8 % (26 pa- chiatry: pharmacological treatment and . tients). There was significant difference between pretreat- Pharmacological treatment employs drugs to reduce psy- ment and posttreatment CGI scores (\.001), and the self- chiatric symptoms, and its effectiveness varies across dis- orders and medications. Antidepressant medications, when used as a monotherapy in placebo-controlled registration E.-J. Cheon Á B.-H. Koo (&) Á W.-S. Seo Department of Psychiatry, Yeungnam University Medical trials, typically result in 30–35 % remission rates (Rush Center, Yeungnam University College of Medicine, 317-1, et al. 2011). Psychotherapy includes psychodynamic psy- Daemyeong 5-dong, Nam-gu, Daegu, Republic of Korea chotherapy and cognitive behavioral therapy. The effect of e-mail: [email protected] cognitive behavioral therapy is similar to that of pharma- J.-Y. Lee cotherapy, although the effect size is small (Lynch et al. Department of Psychiatry, CHA Gumi Medical Center, 2010). Psychodynamic psychotherapy shows empirical ef- CHA University, Gumi, Republic of Korea fectiveness, although there is some difficulty in verifying it through experimental studies (Cuijpers et al. 2008). How- J.-H. Choi Department of Psychology, Yeungnam University Medical ever, there is an unmet need for such conventional treat- Center, Yeungnam University College of Medicine, Daegu, ment methods. Pharmacological treatment methods can Republic of Korea lead to adverse outcomes such as dry mouth, headache, nausea, constipation, and sexual dysfunction, which can S.-H. Song Department of Psychiatry, Daedong Hospital, Daegu, Republic hamper the patient’s treatment compliance and quality of of Korea life (Lam et al. 2009). To enhance treatment effectiveness 123 18 Appl Psychophysiol Biofeedback (2015) 40:17–24 and address the limitations of conventional methods, many epilepsy, and other organic mental disorders were excluded complementary treatments have been proposed, among from the study. which neurofeedback is one of the most sophisticated method. Experimental Procedure EEG biofeedback, known as neurofeedback, is an operant conditioning procedure in which patients learn to Patients who met inclusion and exclusion criteria of the improve the brain’s functional activity (Larsen and Sherlin study were referred to the neurofeedback clinic by the at- 2013; Weiskopf et al. 2004). It is an active training pro- tending . The patients were evaluated during gram in which the individual can restore the regulation of weekly neurofeedback team meetings with three psy- the brain network, spontaneously (Johnston et al. 2010; chiatrists and a neurofeedback therapist. The neurofeed- Weiskopf et al. 2004). Since 1960, neurofeedback has been back protocol was determined by certified in verified to be effective in epilepsy and applied to various neurofeedback during the neurofeedback team meeting for fields. In addition, its potential to be used to elucidate the each patient. This decision took into account the patient’s mechanisms underlying psychopathology by evaluating the chief complaints, opinions of the attending psychiatrist at subjective effect of the modulation of specific brain areas the outpatient clinic, neuropsychiatric evaluation results, has become apparent (Linden et al. 2012; Moriyama et al. and the subjective-symptom-rating scale. Outcomes of 2012; Sterman et al. 1974). In psychiatry, neurofeedback neurofeedback treatment were reviewed by the psychiatrist has been used in attention deficit hyperactivity disorder specializing in neurofeedback, and feedback was provided (Moriyama et al. 2012), depressive disorders, anxiety dis- to each patient. In addition, an appropriate treatment pro- orders (Hammond 2005), sleep disorders (Arns and tocol was arranged as needed. As a retrospective study, Kenemans 2014; Cortoos et al. 2009), substance abuse patient consent was exempted, and this study was approved (Sokhadze et al. 2008), the cognitive rehabilitation of by the hospital ethics committee. patients with head trauma or cerebrovascular disorders (Angelakis et al. 2007; Thornton 2000). In addition, it has Measures been used to improve performance (peak performance) in normal individuals (Vernon 2005). Demographic data, the patient’s psychiatric history, and the There is sufficient evidence supporting neurofeedback neurofeedback training protocol were recorded. The pri- treatment in epilepsy (Sterman et al. 1974), attention deficit mary measure of treatment effectiveness was the clinical hyperactivity disorder, and substance abuse (Moriyama global impression-severity (CGI-S) scale, which is a et al. 2012; Sokhadze et al. 2008), but few well-controlled widely used tool in the objective rating of treatment ef- studies have considered neurofeedback treatment in adult fectiveness. It is rated on the following seven-point scale: psychiatric patients. In this regard, the present study in- 1 = normal, not at all ill; 2 = borderline mentally ill; vestigates the characteristics and effects of neurofeedback 3 = mildly ill; 4 = moderately ill; 5 = markedly ill; on adult psychiatric patients in a naturalistic setting. 6 = severely ill; 7 = among the most extremely ill pa- tients. The CGI can track clinical progress across time and has been shown to correlate with longer, more tedious and Materials and Methods time consuming rating instruments across a wide range of psychiatric diagnoses. It has shown good inter-rater Participants reliability and validity, and recently published guidelines improved the precision of CGI scoring (Busner and Tar- The participants were enrolled from a population of pa- gum 2007; Busner et al. 2009). The CGI ratings were de- tients with neurofeedback treatment at an outpatient clinic termined during weekly neurofeedback team meetings with of the psychiatric department of a university hospital from attending psychiatrists from the outpatient clinic and those August 2005 to August 2009. A total of 77 adult patients psychiatrists in charge of the initial planning and super- whose ages exceeded 18 were recruited. For inclusion in vising the progress of neurofeedback treatment and we the study, patients had to meet DSM-IV-TR criteria for found significant inter-rater correlation (Kappa [ .90). Axis I disorder (American Psychiatric Association and The secondary measure of treatment effectiveness was American Psychiatric Association Task Force on DSM-IV the Hill–Castro checklist for the subjective rating of 2000). They could communicate with the evaluator and symptom improvement. For the patient’s better under- consented to participate in neurofeedback training. Patients standing, the visual analog scale (VAG) was adopted. This with low tolerability with medications or unsatisfactory checklist includes the following psychiatric symptom treatment response were regarded suitable candidate. categories: depression, anxiety, hostility, sleep, impul- Patient with dementia, mental retardation, head trauma, sivity, hyperactivity, attention, self-esteem, immaturity, 123 Appl Psychophysiol Biofeedback (2015) 40:17–24 19 masochism, and tic, and others. The checklist provides adjustment disorders, bipolar disorder, , attention percentages, not cutoff scores, and a broader overview of deficit hyperactivity disorder, alcohol dependence, game ad- how a patient is functioning in various areas of his or her diction, and impulse control disorder. The most common di- life (Hill and Castro 2002). agnosis included was depressive disorders (24.7 %), followed by anxiety disorders (23.4 %). Anxiety disorders included Neurofeedback Apparatus generalized anxiety disorder, , obsessive–com- pulsive disorder, social phobia, acute stress disorder, and The neurocybernetics model of neurocybernetics company posttraumatic stress disorder. The duration of illness ranged was used for neurofeedback training. The brain’s electrical from\2to[6 years. Most of the patients (89.6 %) currently activity was displayed on a monitor in the form of an au- received psychiatric pharmacological treatment, and the du- diovisual exercise. In the SMR or beta training protocol, ration of treatment ranged from\2to[4 years. the patients were introduced a computer game, and reward feedback was represented as achievement scores and graphs during and after training. In the alpha-theta training Neurofeedback Treatment State protocol at the Pz area, the patients sat in a chair with eyes closed, and only audio feedback was provided. In SMR Table 2 shows the neurofeedback treatment protocol. The training, the reward band ranged from 12 to 15 Hz, and in average frequency of neurofeedback treatment was beta training, from 15 to 18 Hz. In alpha-theta training, the 17.39 ± 16.64. A total of 39 patients (50.6 %) received patients were trained simultaneously to reduce alpha and neurofeedback treatment more than 10 times. A total of 26 increase theta to the point at which they ‘crossed over’, patients received less than 5 sessions. The patients belongs which was defined as the point at which the alpha ampli- to the group, who took 6–10 sessions of treatment, were 9, tude dropped below the level of theta (Dehghani-Arani 11–15 sessions were 8, 16–20 sessions were 6. The patient et al. 2013). The theta (5–8 Hz) and alpha (8–12 Hz) were who received more than 20 sessions of treatment was 25. reward bands. Before and during training, the participants The neurofeedback protocol was beta, sensorymotor were instructed to develop the most successful mental rhythm (SMR), and/or alpha-theta training. The protocol strategy to get as much reward feedback as possible. combining alpha-theta training with either beta or SMR training was the most common method (62.3 %). The re- Statistics gions of the brain where neurofeedback was applied to were Fp1, Fp2, F3, F4, F7, F8, T3, T4, C3, C,4, P1, P2, O1, A frequency analysis and a technique analysis were con- O2, and Oz based on the international 10–20 EEG system ducted to examine the patients’ demographic characteris- (Herwig et al. 2003). A total of 49 patients (63.6 %) were tics and clinical features. To examine the effect of treated in more than two brain regions. The discontinuation neurofeedback on the patients, a paired t test was con- rate for neurofeedback treatment was 33.8 %. The dis- ducted based on changes in pre-treatment and post-treat- continuation was defined as ending therapy without pre- ment CGI scores as an objective index and on changes in scription of attending psychiatrist or lost to follow up. the Hill–Castro checklist as a subjective index, setting time In this study, the neurofeedback protocol was not uni- as a covariant. PASW version 18.0 for Windows (Chicago, form according to the diagnosis. For example, in those IL) was used for all statistical analyses. The level of sig- patients with depressive disorders, their chief complaints nificance in each analysis was set to .005 with Bonferroni ranged from anxiety, agitation, and emotional unstability to correction procedure. lethargy, reduced energy, concentration difficulties, and thought distortion. The treatment protocol was adjusted according to each patient’s chief complaints, the treatment Results goal of the attending psychiatrist, and outcomes for the subjective-symptom-rating scale. In those patients with Demographic Data and Clinical Characteristics anxiety disorders, alpha–theta training was chosen, and an individualized protocol was selected during the neuro- Table 1 summarizes the demographic data and clinical feedback meeting. Those patients showing a low threshold characteristics of the sample. Among the 77 patients, 40 for anxiety were treated with SMR training at T4 and al- (51.9 %) were male. The patients’ ages were evenly dis- pha-theta training at Pz at first. When their anxiety level tributed, with 36 (46.8 %) in their thirties and forties (the decreased after neurofeedback treatment, beta training was largest age group). introduced at F3. In sum, the treatment protocol was in- The patients received neurofeedback for depressive disor- dividualized and finalized during weekly neurofeedback ders, anxiety disorders, sleep disorders, somatoform disorders, meetings. 123 20 Appl Psychophysiol Biofeedback (2015) 40:17–24

Table 1 Demographic data and Variables Groups N (%) clinical characteristics (n = 77) Sex Male 40 (51.9) Female 37 (48.1) Age (mean ± SD) 10’s to 20’s 24 (31.2) 30’s to 40’s 36 (46.8) 50’s to 6o’s 13 (16.9) 70’s to 80’s 3 (3.9) 39.86 ± 15.46 Education (mean ± SD) Years B 9 7 (9.1) 9 \ years B 12 29 (37.7) Years [ 12 36 (46.8) 13.78 ± 2.70 Diagnosis Depression 19 (24.7) Anxiety disorder 18 (23.4) Sleep disorder 8 (10.4) Somatoform disorder 6 (7.8) Adjustment disorder 5 (6.5) Bipolar disorder 4 (5.2) ADHD 3 (3.9) Game addiction 3 (3.9) Psychosis 3 (3.9) Other psychiatric disorders 6 (7.8) Duration of illness (years) Years B 2 32 (41.6) 2 \ years B 4 34 (44.2) 4 \ years B 6 4 (5.2) Years [ 6 4 (5.2) Presence of medication Presence 69 (89.6) Not presence 7 (9.1) Duration of medication (years) Years B 2 35 (45.5) 2 \ years B 4 18 (23.4) Years [ 4 16 (20.8)

Table 2 States of EEG Variables Groups N (%) biofeedback Frequency (mean ± SD) Total 74 (17.39 ± 16.64) 1–5 26 (2.73 ± 1.28) 6–10 9 (7.56 ± 1.33) 11–15 8 (13.13 ± 1.25) 16–20 6 (17.50 ± 1.64) [20 25 (37.52 ± 11.89) Protocol b/SMR 6 (7.8) a/h 19 (24.7) Both b or SMR and a/h 48 (62.3) Region Only one region 23 (29.9) Over two regions 49 (63.6) Discontinuation rate 26 (33.8)

123 Appl Psychophysiol Biofeedback (2015) 40:17–24 21

Neurofeedback Effectiveness by CGI Scores 21 clinical studies reported on neurofeedback treatment in patients with depressive disorders, and there have been The average pre-treatment CGI score was 2.99 ± 1.54, and only six original articles. These studies were not controlled the average post-treatment CGI score was 1.88 ± 1.57. and included fewer than 15 patients (Baehr et al. 1997, There were significant decreases in the severity of symp- 2001; Earnest 1999; Hammond 2000; Rosenfeld 1997), and toms after treatment (\.001). all reported positive results (Baehr et al. 1997, 2001; Earnest 1999; Hammond 2000; Rosenfeld 1997). The most Neurofeedback Effectiveness by the Hill–Castro Checklist Score Table 3 Effects of neurofeedback by pre-treatment and post-treat- ment the Hill–Castro checklist (n = 22) Figure 1 and Table 3 show the pre-treatment and post- Variables Mean ± SD t (p) treatment Hill–Castro checklist scores. The Hill Castro Checklist score was given to all the patients who received Attention 54.59 ± 19.04 4.33 (.0001) neurofeedback treatment at baseline and the end of the 38.68 ± 21.70 treatment. Only 22 patients were responded both at base- Hyperactivity 47.59 ± 19.36 3.21 (.004) line and the end of the treatment. There were significant 34.09 ± 24.06 improvements in depression (.0001), anxiety (.0001), self- Impulsivity 38.27 ± 20.22 3.12 (.005) esteem (.0001), hostility (.0001), attention (.0001), hyper- 26.55 ± 20.05 activity (.004) after treatment, but no significant changes Immaturity 35.64 ± 23.26 3.15 (.005) were observed for other scales. 22.86 ± 17.94 Hostility 37.14 ± 17.99 4.45 (.0001) 24.55 ± 18.85 Discussion Masochism 9.27 ± 11.19 1.12 (.277) 7.23 ± 12.81 This study evaluates the characteristics and effects of Tic 16.41 ± 16.65 2.32 (.030) neurofeedback on adult patients with psychiatric disorders 10.82 ± 15.45 in a naturalistic setting. Depression 54.50 ± 20.75 6.11 (.0001) In the present study, the most common for 31.68 ± 24.68 neurofeedback treatment included depressive disorders. In Anxiety 51.95 ± 20.46 7.32 (.0001) EEG studies of depression, an abnormal pattern of asym- 26.86 ± 19.01 metric activity in the frontal regions from relative hyper- Self-esteem 41.64 ± 20.13 4.28 (.0001) activity over the right frontal regions and/or relative 28.73 ± 21.79 hypoactivity over the left frontal regions has frequently Sleep 34.41 ± 23.53 2.39 (.026) been observed (Henriques and Davidson 1990). A neuro- 25.09 ± 24.15 feedback protocol for modifying this frontal asymmetry Others 38.89 ± 13.69 5 (.0001) has been proposed (Rosenfeld 2000; Rosenfeld et al. 1995). 21.21 ± 17.27 According to the recent paper (Dias and van Deusen 2011),

Fig. 1 Effects of 70 neurofeedback by pre-treatment Baseline End and post-treatment the Hill– 60 Castro checklist. *p \ .005 50

40

30

20

10

0

Tic Sleep Hostility* Anxiety* Others* Attention* ImpulsivityImmaturity Masochism Depression* Hyperactivity* Self-esteem*

123 22 Appl Psychophysiol Biofeedback (2015) 40:17–24 commonly used protocol focuses on alpha inter-hemi- use of EEG feedback to reduce anxiety by reducing alpha spheric asymmetry and the theta–beta ratio for the left activity and increasing beta activity and found that neither prefrontal cortex (Dias and van Deusen 2011). Choi et al.’s should be used as a uniform protocol for treating anxiety (2011) pilot study is the first randomized controlled trial disorders but that each case should be planned individually examining whether alpha asymmetry neurofeedback train- depending on the patient’s history and baseline EEG pat- ing can improve symptoms in patients with depressive terns. They suggested that finding some balance in the EEG disorders. Earlier findings suggesting that enhancing the pattern may be more important than increasing or reducing left frontal activity alleviates depressive symptoms were EEG alpha and called for a controlled study using a larger replicated, and cognitive tests showed that asymmetry population for a differential approach to neurofeedback training improved the performance of executive functions, (Thomas and Sattlberger 1997; Plotkin and Rice 1981). In whereas placebo treatment, no improvement. The Roshi the present study, individualized protocols were deter- (Hammond 2000) protocol is another protocol for neuro- mined during neurofeedback meetings for patients with feedback treatment in patients with depression. This pro- anxiety disorders. According to the patient’s chief com- tocol is a two-channel unit combining neurofeedback with plaints and baseline readings from the neuropsychiatric photic stimulation based mainly on the beta training of the evaluation and the subjective-symptom-rating scale, beta at left hemisphere. In the case study, the initial session of T3 or F3 or SMR at T4 and/or alpha–theta at Pz was se- EEG neurofeedback using Rosenfeld’s protocol was dis- lected. For example, a sequential treatment protocol with couraging, and therefore the treatment protocol was shifted 10 initial sessions of SMR at T4, followed by 10 sessions to the Roshi protocol for the beta training of the left of beta training at F3, was applied. Previous studies en- hemisphere. According to the results, patients became less rolled volunteers reporting chronic anxiety, but they were withdrawn and more active after 30 training sessions not psychiatric patients diagnosed with anxiety disorders (Hammond 2000). In the present study, the treatment according to the DSM. In the present study, only those protocol for depressed patients was not uniform but indi- patients diagnosed with axis I disorders in a clinical setting vidualized. The patient’s most serious symptoms were were recruited. considered for preferential treatment, and the protocol was Other than depression and anxiety, our study also in- discussed and adjusted during weekly neurofeedback cluded sleep disorder, somatoform disorder, adjustment meetings. For depressed patients, correcting any abnormal disorder, bipolar disorder, ADHD, game addiction and pattern of asymmetric activity in the frontal regions and psychosis patients. There were studies that report positive recovering balance in their brain activity played important results of neurofeedback treatment on sleep disorder (Arns roles in reducing depressive symptoms regardless of whe- and Kenemans 2014; Cortoos et al. 2009), substance abuse ther the Rosenfeld or Roshi method was employed. De- (Peniston and Kulkosky 1989; Saxby and Peniston 1995; pressed patients with severe anxiety symptoms were Scott et al. 2005) and ADHD (Moriyama et al. 2012). treated with SMR at T4 and alpha–theta at Pz. After their There were few studies about neurofeedback treatment on serious anxiety symptoms were addressed, treatment goals psychosis patients or bipolar disorder. Even though the and protocols were revised to alleviate depression by beta sample size was small, our study results suggested that training at F3. On the other hand, depressed patients whose neurofeedback treatment could alleviate clinical symptoms chief complaints were energy loss and concentration dif- in patients with variety of psychiatric conditions. ficulties were provided with neurofeedback training start- In the present study, neurofeedback could decrease the ing with beta training at either T3 or F3. severity scores of the CGI effectively. The standard CGI is The second most common disease in this study included used in virtually all FDA-regulated and most other CNS anxiety disorders. There were studies of neurofeedback trials. And it is regarded effective if certain medication or treatment in generalized anxiety disorder, phobic disorder, treatment method could decrease severity score of CGI by obsessive–compulsive disorder, post-traumatic stress dis- more than one point (Busner and Targum 2007; Busner et al. order, and panic disorder. Most studies considering anxiety 2009). disorders have been case reports with small numbers of Neurofeedback treatment improved depression, anxiety, subjects, and there is no large, well-controlled study self-esteem, hostility, attention, and hyperactivity based on (Moore 2000). Thomas and Sattelberger (1997) treated six the Hill–Castro checklist. The exact mechanism underlying chronic anxiety patients with neurofeedback and found an its effect on the patients could not be elucidated, but increase in EEG alpha to be beneficial only for patients changes not only in mood- and anxiety-related symptoms showing low-amplitude alpha. Those patients with anxiety but also in personality and cognition could be the potential showing abnormally high levels of alpha at baseline read- mechanism. Peniston and Kulkosky (1989) found person- ings did not respond effectively to alpha increase neuro- ality changes after alpha-theta neurofeedback treatment in feedback. Their case report attempted to demonstrate the patients with substance dependence but not in the control 123 Appl Psychophysiol Biofeedback (2015) 40:17–24 23 group with conventional treatment. Neurofeedback treat- Busner, J., Targum, S. D., & Miller, D. S. (2009). The Clinical Global ment was also considered in the cognitive rehabilitation Impressions scale: Errors in understanding and use. Compre- hensive Psychiatry, 50(3), 257–262. (Angelakis et al. 2007; Thornton 2000) and could facilitate Choi, S. W., Chi, S. E., Chung, S. Y., Kim, J. W., Ahn, C. Y., & Kim, the function of the left frontal lobe in major depressive H. T. (2011). Is alpha wave neurofeedback effective with disorder (Choi et al. 2011). randomized clinical trials in depression? A Pilot Study. The present study has some limitations. First, there was Neuropsychobiology, 63(1), 43–51. Cortoos, A., Valck, E., Arns, M., Breteler, M. H. M., & Cluydts, R. no control group, and the possibility of positive outcomes (2009). An exploratory study on the effects of tele-neurofeed- being due merely to the participants’ belief that they were back and tele-biofeedback on objective and subjective sleep in being treated cannot be ruled out. Second, most patients patients with primary insomnia. Applied Psychophysiology and were already receiving pharmacological treatment, and its Biofeedback, 35(2), 125–134. Cuijpers, P., van Straten, A., Andersson, G., & van Oppen, P. (2008). effects on their symptoms were not controlled for. Third, Psychotherapy for depression in adults: A meta-analysis of the patients were not homogenous, and various psychiatric comparative outcome studies. Journal of Consulting and disorders were included. Finally, the treatment protocol Clinical Psychology, 76(6), 909–922. was determined according to the patient’s subjective Dehghani-Arani, F., Rostami, R., & Nadali, H. (2013). 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