The 4th IEEE International Conference on E-Health and Bioengineering - EHB 2013

Grigore T. Popa University of Medicine and Pharmacy, Iaşi, Romania, November 21-23, 2013

978-1-4799-2373-1/13/$31.00 ©2013 IEEE

Evaluation of Emotional Influence on EEG Activity in the Frontal Lobes

Bogdan-Andrei Tăbăcaru Faculty of Medical Engineering, University “Politehnica” of Bucharest

Bucharest, Romania Dept. DES DMF SLV, Infineon Technologies AG

Neubiberg, Germany Bogdan-Andrei.Tabacaru@infineon.com

Abstract—the electroencephalographic (EEG) activity is analyzed here to detect alpha rhythms asymmetry related to induced depression; EEG signals were acquired from the frontal lobes. Seven young subjects, students of similar age, voluntarily participated in the experiment. The initial emotional state of the subjects was assessed by three independent questionnaires, designed for psychological evaluation of depression and the results were compared. Several sequences of recordings were taken afterward (base, induced happiness, and induced sadness). The left dominant alpha-asymmetry (LDAA) index was calculated for each EEG recording. The outputs were analyzed and compared with similar assessments presented in the scientific literature, leading to similar conclusions, i.e. stimulated happiness lowers the LDAA index and stimulated sadness raises the LDAA index. The results also suggested that the repetition of the process tends to lower personal index values from one session to another.

Keywords—Electroencephalogram; Alpha asymmetry; Depression; Emotion; Signal-processing

I. INTRODUCTION

Depression, as well as anger, is a complex state of the human mind [1]. These states are strongly connected to the brain’s limbic system and the adrenal glands as well. The presented study uses a non-invasive brainwave measuring technique, electroencephalography (EEG), for the analysis of the limbic system’s effects on the brain especially in the frontal lobes.

Previous studies [2] have documented that there is a significant difference between the electroencephalographic activity of depressed and non-depressed persons. One study had analyzed the influence of emotions on the dorsolateral lobes [3]. However, no relative differences were observed between healthy and non-healthy subjects. The notion that alpha waves correspond to cerebral hypo-activation, and beta waves correspond to cerebral hyper-activation was introduced by [4]. Rosenfeld et al. were the first to show that a subject could control the asymmetry degree of alpha-waves between the two frontal lobes when operant conditioning was used.

Although the analysis of alpha asymmetry levels was highly accepted in the beginning, other studies were not able to produce the same results as in [5]. Because of this, Coan and

Allen proposed that emotions should be stimulated in a subject [6].

This paper proposes a very simple and efficient method for processing EEG recordings, which could be integrated in a neurofeedback training protocol for the assessment of the therapeutic progress. The study performed here is meant to evaluate the relevance of the EEG signal’s determined indicators.

II. METHOD

A. Subjects All subjects participating in the study are right-handed

Caucasian adult university students. They are representatives of both sexes. Their age ranged from 22 to 25 years old. One of the subjects was excluded from the study because he was outside the age range (34 years old). All students participated as volunteers and were not recompensed in any way. No legal binding was imposed for any subject; they were free to leave the study whenever they wished. Five subjects took part in all 3 recording sessions; two subjects only underwent the first session. B. Data Acquisition

The EEG recordings have been conducted using the data acquisition system BIOPAC MP30/35. The EEG sensors were placed according to the International 10-20 System for placing EEG electrodes. The area of interest was at points F3 and F4 (in the frontal lobes). The recording montage was made referential. One pair of ground and reference sensors was placed on each earlobe and the second on the left and right parts of the lower-jaw, because the acquisition system (designed for differential measurements) did not permit placement of common ground and reference sensors. The electrodes were EL503. These passive, disposable, surface sensors are 10mm in diameter and made from Ag-AgCl. They were connected to the BIOPAC system using SS2L connectors. No extra conductive gel has been used because the sensors came with an already applied layer.

Two channels were used to record the electrical activity at positions F3 and F4. The sampling frequency was 200 Hz. A

numerical band-pass filter with cutting frequencies 0.5 – 35 Hz was used for the 2 channels. Another band-stop filter centered on the power-line interference frequency of 50 Hz (Q=1) was used. A hardware amplification of 25000 with offset 0 mV and an analog band-pass filter with frequencies 0.5 Hz – 1 kHz were also used.

The alpha waves were filtered using a numerical band-pass filter (8-13 Hz, Q=0.707) for each recorded channel. Finally, the alpha-power waves were calculated for each recording channel as being the squared value of the alpha-wave signal.

C. Procedure

Each subject was required to attend 3 recording sessions. Each recording session was 2 weeks apart from the other. The subjects were also required to fill-in 3 depression self-assessment questionnaires Hamilton Rating Scale for Depression (HAM-D), Beck’s Depression Inventory (BDI) and Interview to Diagnose Depression (IDD) before each session. Next, they took part in 3 recording phases: baseline recording, negative emotion stimulation, and positive emotion stimulation. One of the subjects refused to take part in the recording phase with negative emotion stimulation.

The subjects who received more than 7 points on HAM-D or 10 points on BDI or IDD questionnaires were considered to be suffering from some form of depression (mild – severe). The others were considered not depressed.

After completing the questionnaires, the subjects were seated on a comfortable chair. They were asked to relax and to make some neck-relaxation exercises. They were instructed not to move during the recording and were recommended to use diaphragmatic breathing and also not to blink (if possible) because EMG artifacts could be involuntarily acquired in the recordings.

Each recording session lasted 60 seconds. During this time the subjects were asked to keep eyes closed or eyes open for 10-second intervals, according to the following sequence succession: eyes-closed (C), eyes-open (O), C, O, C, and O.

The first recording phase was the baseline recording. Afterwards, the subjects were asked to watch a sad video and to let it stimulate them emotionally. They were also asked to remember and try to relive a very sad experience from their lives as vividly as possible. Next, came the negatively-stimulated recording. Afterwards, the subjects were asked to watch a funny video and try to relive a very happy event from their lives as vividly as possible. Finally, the positively-stimulated recording took place.

D. Data Analysis

The EEG recordings were analyzed after each session was concluded. The alpha-power waves for F3 and F4 have been used for the analysis. The recordings were stripped from all artifacts. Each 1 second interval from a recording was transformed into 1 epoch using a rectangular filter with 0% over-lapping. All epochs were normed after their maximum mean value. The asymmetry index (1) was calculated for

each epoch [7]. L and R are the mean values of the alpha-power wave from F3 and F4, respectively.

A = ln(L) – ln(R). (1)

The A-scores were normed after the longest recording of

each session. Finally, the left-dominant alpha-asymmetry (LDAA) index was calculated as the percentage of a whole recording in which the A-score had a negative value.

III. RESULTS

The scores for each subject’s questionnaires are specified in Table I. They are added for each session in which the subject took part and is referenced to the LDAA’s value for the baseline recording. Two subjects left the study after the first recording session.

The LDAA values which each subject received after the analysis of every session’s recording are specified in Table II.

TABLE II. LDAA VALUES FOR EACH SUBJECT’S RECORDING SESSIONS Subject Session LDAA

for baseline

LDAA for stimulated sadness

LDAA for stimulated happiness

A.F. 1 36.96 43.48 2.17 A.V. 1 21.74 73.91 28.26 B.C. 1 54.55 - 20.45 C.V. 1 71.43 - 55.10 I.S. 1 20.45 56.82 18.18

M.B. 1 73.33 55.56 53.33 O.L. 1 9.52 38.10 33.33 A.F. 2 19.05 50 52.38 A.V. 2 19.15 23.40 12.77 B.C. 2 15.56 24.44 13.33 C.V. 2 10.42 - 41.67 M.B. 2 13.04 28.26 39.13 A.F. 3 21.95 24.39 65.85 A.V. 3 82.22 86.67 44.44 B.C. 3 21.57 47.06 25.49 C.V. 3 26.32 - 10.53 M.B. 3 8.89 17.78 22.22

TABLE I. QUESTIONNAIRE SCORES FOR EACH SUBJECT’S RECORDING SESSIONS

Subject Session LDAA for baseline

HAM-D BDI IDD

A.F. 1 36.96 3 0 0 A.V. 1 21.74 11 13 10 B.C. 1 54.55 9 10 5 C.V. 1 71.43 5 12 7 I.S. 1 20.45 4 3 1

M.B. 1 73.33 18 13 2 O.L. 1 9.52 8 7 4 A.F. 2 19.05 0 0 0 A.V. 2 19.15 7 4 3 B.C. 2 15.56 12 9 4 C.V. 2 10.42 2 0 6 M.B. 2 13.04 1 4 2 A.F. 3 21.95 0 1 0 A.V. 3 82.22 11 8 5 B.C. 3 21.57 6 6 2 C.V. 3 26.32 0 0 0 M.B. 3 8.89 1 3 0

They are added for each session in which the subject took part and is referenced to the LDAA’s value for the baseline recording. Subject C.V. requested not to take part in the recordings of stimulated sadness. Subject B.C.’s stimulated sadness recording from the first session was corrupted and was deemed unusable.

The p-values for the LDAA values of each recording, as well as for the scores of each questionnaire are specified in Table III. The p-values were calculated using the Chi-Squares algorithm.

A. Group discussion

As per Table I, 14 out of 17 (82.35%) results show that the LDAA value from the baseline recordings is smaller than 50% in subjects who obtained questionnaire scores that do not indicate any form of depression and greater than 50% in those subjects for which the questionnaires indicated some form of depression (mild-severe).

As per Table II, 12 out of 13 (92.30%) results show LDAA values from the stimulated sadness recordings, which are greater than the LDAA values from the same subject’s baseline recordings.

As per Table II 9 out of 17 (52.94%) results show LDAA values from the stimulated happiness recordings, which are smaller than the LDAA values from the same subject’s baseline recordings. However, 13 out of 17 (76.47%) results show LDAA values smaller than 50%, regardless of existing or inexistent depression forms. In addition, 9 out of 13 (69.23%) results show that the LDAA values are smaller than the corresponding LDAA values from the stimulated sadness recording.

B. Session discussion

Session 1 Three out of seven (42.85%) subjects presented LDAA

values greater than 50% in the baseline recordings. Four out of seven (57.14%) subjects obtained

questionnaire scores, which indicate mild depression. The rest received scores indicating no trace of depression.

Three out of seven (42.85%) subjects recorded obtained LDAA values greater than 50% in the stimulated sadness recordings; 4 out of 7 (57.14%) subjects obtained LDAA values greater than those in the baseline recording.

Five out of seven (71.42%) subjects obtained lower LDAA values in the stimulated happiness recording than in the baseline recording.

Session 2 Four out of five (80%) subjects recorded lower scores

at the questionnaires. All subjects recorded lower LDAA values in the

baseline and stimulated happiness recordings than in the previous session.

Four out of five (80%) subjects obtained greater LDAA values in the stimulated sadness recording than in the baseline recording.

Session 3 Only 1 subject (20%) obtained greater scores in all

questionnaires than in the previous session. The HAM-D score of 8 is indicative of mild depression for subject A.V.

All subjects except for A.V. obtained lower LDAA values in the baseline and stimulated happiness recordings, than in the previous session.

IV. CONCLUSIONS

Presently, the topic of alpha asymmetry using for diagnosing depression in a subject is still fairly controversial. However, the results offered in the present paper support this hypothesis.

The results presented in this paper show that the LDAA value is correlated with the scores obtained in the depression self-assessment questionnaires. This means that for a LDAA value greater than 50%, the subject obtained a depression indicative score in at least 1 questionnaire.

This small time frame in which the subjects had to recover from the negatively-stimulated emotion and undergo the positively-stimulated emotion might not have been sufficient for them to fully recover and thus the LDAA values for the stimulated happiness recording could have been affected.

It was shown that the LDAA value is dependent on the subject’s emotion. The LDAA value raises when the subject is stimulated negatively (induced sadness) and drops below the 50% limit when the subject is stimulated positively (induced happiness).

It has been also shown that the subjects’ positive (happiness) or negative (sadness) emotions influence their brain-wave activity in the frontal lobes.

The results show a mild tendency of the LDAA values as much as the questionnaire scores to drop from the previous recording session to the next, which might be the result of the subjects' adaptability to the tests and their rising emotional involvement. Although the analysis of the recordings’ positive effects was not the main goal of this paper, this aspect should not be overlooked.

All the subjects involved in the experiment are healthy young people with no diagnosis and/or psychological problems. They have only acted as test subjects reacting, as natural as possible and with all their benevolence and sincerity, to harmless voluntarily applied stimuli, for inducing

TABLE III. P-VALUES FOR LDAA VALUES AND QUESTIONNAIRE SCORES LDAA

for baseline

LDAA for stimulated

sadness

LDAA for stimulated happiness

HAM-D BDI IDD

p<0.001 p<0.001 p<0.002 p<0.001 p<0.0011 p<0.001

sadness and happiness feelings. The results of the study gain therefore significance and they show a strong potential for LDAA as a reliable index for emotional state identification and monitoring in real patients, especially for the evaluation of the efficiency and progress during certain applied therapy.

Finally, the proposed method and the evaluated LDAA values seem appropriate to be integrated and used within a neurofeedback anti-depressive training protocol.

ACKNOWLEDGMENT

The author would like to thank Prof. Mihaela Morega for guidance and advice throughout the research program and to acknowledge the working environment provided by the Faculty of Medical Engineering of UPB and by Infineon Technologies AG.

REFERENCES [1] Siao Zheng Bong, M Murungappan and Sazali Yaacob, “Methods and

approaches on inferring human emotional stress changes through physiological signals: a review,” Int. J. Medical Engineering and Informatics, 5 (2), 2013

[2] Ian H. Gotlib, Charan Ranganath, and J. Peter Rosenfeld, “Frontal EEG Alpha Asymmetry, Depression, and Cognitive Functioning,” Cognition and Emotion, 12 (3), pp. 449-478, 1998.

[3] R. J. Davidson, C. E. Schaffer, and C. Saron, “Effects of lateralized presentations of faces on self-reports of emotion and EEG asymmetry in depressed and non-depressed subjects,” Psychophysiology, 12 (3), pp. 353-364, 1985.

[4] R. J. Davidson, “Anterior cerebral asymmetry and the nature of emotion,” Brain and Cognition, 20, pp. 125-151, 1992.

[5] J. P. Rosenfeld, G. Cha, T. Blair, and I. H. Gotlib, “Operant (biofeedback) control of left-right frontal alpha power differences,” Biofeedback Self-Regulation, 20 (3), pp. 241-258, 1995.

[6] James A. Coan, John J. B. Allen, and Patrick E. McKnight, “A capability model of individual differences in frontal EEG asymmetry,” Biological Psychology, 72, pp. 198-207, 2006.

[7] Elsa Baehr, J. Peter Rosenfeld, Rufus Baehr, and Carolyn Earnest, “Comparison of two EEG asymmetry indices in depressed patients vs. normal controls,” International Journal of Psychophysiology, 31, pp. 89-92, 1998