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Home , Emotion perception

Relationship among Generalized and auditory : An EEG Frontal

Alpha Asymmetry study

Theresa Jane Hamm

ANR: 2005308

Supervisor: Jeroen Stekelenburg

Liberal Arts and Sciences: Major

Tilburg University

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY

Abstract

Individuals demonstrate significant differences in their response and interpretation towards affective stimuli. Hemispheric alpha asymmetry has been hypothesized as an indication of emotional and motivational behavior. Abnormal emotional perception and motivational tendencies, such as those exhibited in generalized anxiety disorder, have been linked to relative right sided frontal electroencephalograph (EEG) asymmetry. On the basis of prior theory and research, the current study hypothesized that individuals with self-reported generalized anxiety

(GAD) would exhibit distinct FAA patterns (i.e. greater relative right frontal activity; relatively diminished right alpha power) compared to healthy individuals. Such FAA patterns were expected during rest and when confronted with negative affective stimuli. Using EEG experimentation, individual emotional perception and resting FAA was measured. Results demonstrated that no differences in FAA were present between those with significant GAD scores and healthy individuals.

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY

Approximately one out of 14 individuals worldwide meet the diagnostic criteria for anxiety (Baxter, 2013). More specifically, the most frequent anxiety disorder found in primary care is generalized anxiety disorder (Jordan et al., 2017). A general population survey, conducted over 26 different countries, found that generalized anxiety disorder (GAD) has a combined lifetime prevalence of about 3.7% and a 30-day prevalence of approximately 0.08% (Ruscio et al., 2017).

According to the criteria of the Diagnostic and Statistical Manual of Mental Disorders

(DSM), GAD is characterized by a variety of symptoms including but not limited to: restlessness, fatigue, concentration difficulty, , muscle tension, and sleep disturbances

(American Psychiatric Association, 2013). Another common symptom of anxiety is abnormal emotional perception (Mennin et al., 2005; Turk et al., 2005). For example, Turk et al., (2005) found that individuals with GAD performed worse on tests of emotional understanding and emotional negative reactivity when compared to healthy controls. Impaired emotional perception in GAD is an important symptom to highlight as it plays a vital role in human communication and initiating action, both of which are necessary for survival. Additionally, studies have shown that having anxiety may cause a biased vigilance towards threatening stimuli (Bradley et.al.,

1999). Borkovec et al, (2004) suggest that individuals with GAD approach emotional topics at an abstract level, due to increased worrying, which is the central feature of GAD. Consequently, individuals with GAD may avoid intense negative or uncomfortable negative experiences. Such an avoidance response may inhibit effective processing of ‘situationally relevant information’, such as emotions (Novick-Kline et al., 2004). This avoidance is also seen when confronted with aversive images and autonomic . Experiencing , due to GAD, may therefore cause the avoidance of the ‘imagery and physiological arousal’ which accompany

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY negative emotion (Mennin et. al., 2005). Moreover, investigations into the underlying mechanisms of emotional perception suggest that congruence in information provided from facial expressions and affective prosody is what enables behavioral reaction to affective stimuli

(Collignon et al., 2008). Cases of amygdaletomy patients suggest that impairments of emotional recognition occur equally for both processing faces and affective prosody. However, most research investigating emotional perception has been limited to studying the independent role of visual emotional perception as many studies show a ‘visual dominance in the perception of affective expressions’ (Collignon et al., 2008). Few studies investigating perception alone exist; however, Adolphs et al., (2002) did find that lower emotional prosody recognition is mainly associated with right frontal damage. Therefore, it becomes important to understand the individual neurological underpinnings of affective visual and auditory emotional perception when investigating cognitive-behavioral aspects of anxiety.

Through EEG and FMRI studies, researchers have identified distinct neurological differences between healthy individuals and those from GAD. Research into the neurobiology of anxiety disorders found functional hyperactivity in the limbic regions and failure from higher cortical executive areas to properly normalize limbic response to certain emotional stimuli (Martin et al., 2009). For example, structural imaging studies have shown that the upper temporal lobe of pediatric GAD patients consists of high ratios of gray matter to white matter and increased volume (Martin et al., 2009). Considering the detrimental symptoms of

GAD, and its comorbidity with and somatization, improved screening techniques and treatment for GAD is of vital importance for societal health and efficiency (Jordan et al., 2017).

According to Roemer et al., (2002) GAD is considered to be one of the most ‘treatment-resistant’ anxiety disorders. Economic costs of anxiety disorders include reduced work-force productivity,

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY psychiatric/non-psychiatric care, hospitalization, and in extreme cases suicide (Lépine, J., 2002).

Improvements in GAD diagnosis and treatment can be achieved through a deeper understanding of cognitive mechanisms underlying anxiety, specifically those relating to emotional recognition and processing (Wells & Carter, 2001). Further insight regarding the neurological correlates of emotional perception and GAD can be found in studies of frontal alpha asymmetry.

Frontal Alpha Asymmetry

In recent years there has been a growing in the topic of hemispheric lateralization and its relation to emotion and psychopathology, including anxiety. In particular, researchers have been investigating asymmetrical electroencephalographic (EEG) activity over the frontal cortex, both at rest and during certain emotionally charged tasks. The specific activity being investigated in these studies is known as frontal alpha asymmetry (FAA). Here, alpha refers to the brain’s alpha waves, which are most prominent during when one is awake and quietly resting (Enna et al., 2008). Resting EEG FAA investigates ‘trait-like individual differences’ while measurements during emotionally charged tasks aim to investigate FAA with manipulations that influence emotional states (Suo et al., 2017). Therefore, both measurements of FAA can be used to investigate individual differences of emotional experiences. In general, the asymmetric hemispheric difference of alpha activity is computed by subtracting the overall activity in the alpha frequency band (8-12 Hz) at the left electrode from that of the right electrode; this computation is indicative of alpha wave activity experienced in the left and right hemisphere (Thibodeau et al., 2006). Evidence suggests that alpha activity correlates inversely with cortical activity as decreases in alpha are often found when underlying cortical systems engage in active processing; positive values reflect relative increased right alpha power (i.e. less right frontal activity) and negative values reflect relative increased left alpha power (i.e. less left

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY frontal activity) (Coan & Allen, 2004). Whilst conducting an EEG, higher cortical processing tends to be accompanied by reduction in ‘synchronous rhythmic activity’; meaning that relatively greater left or right frontal activity indicates less alpha power in a given region (Van Der Vines et al., 2017). Trends in alpha activity can furthermore be correlated to an individual’s general mental health. Studies that have investigated FAA at rest suggest that relatively greater left frontal activity is psychologically healthier than relatively less left frontal activity (Davidson &

Fox, 1989). Moreover, Su et al., (2017) demonstrated that resting frontal EEG alpha asymmetry was successful in predicting the evaluation of affective stimuli. Investigations into resting FAA and anxiety found individuals with disorders and social phobias demonstrated greater relative right frontal activity when compared to healthy controls (Thibodeau et al., 2006).

Additionally, Wheeler et al. (1993) found that individuals displaying relatively less left- than right-frontal alpha EEG activity show more negative emotional responses to negative films and less positive emotional responses to positive films. Such findings have led to further inquiry into how different emotional and motivational tendencies, as exhibited in GAD, are linked to certain trends in FAA.

EEG, FAA, and Emotion/Motivation Models

Hemispheric alpha asymmetry has been hypothesized as an indication of emotional and motivational behavior. According to Kerson (2002) increased frontal alpha activity is associated with a variety of GAD symptoms such as worry, rumination, and repetitive thinking. This notion can be further explained by the approach-withdrawal model (Briesemeister et al., 2013). This model introduces two motivational systems, approach and withdrawal, which respectively correspond with positive and negative . One of the most prominent symptoms of GAD is excessive worry, which is thought to act as an avoidance or withdrawal function, thereby

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY inhibiting emotional processes (Mennin et al., 2005). Various studies have shown that individuals with GAD exhibited significantly more distress regarding emotions and ‘experiential avoidance’ (Lee et al., 2010; Olatunji et al., 2010). Therefore, as worry promotes avoidance there is an adverse reaction towards negative emotional stimuli (Llera & Newman, 2010). Evidence from EEG studies suggest that left frontal activation corresponds with approach behavior and positive emotion and is interpreted on an EEG by relatively diminished frontal left alpha, compared to right. In contrast, greater right frontal activity corresponds with withdrawal behavior and negative emotion and is represented on an EEG by relatively diminished right alpha, compared to left (Van Der Vinne et al., 2017; Hagemann et al., 2002). These findings can be further supported by evidence of anxious and depressed individuals exhibiting greater relative right than left frontal activity when compared to control groups (Thibodeau et al., 2006).

Gray’s Reinforcement Sensitivity Theory expands on the approach-withdrawal model by introducing the behavioral approach (BAS) and behavioral inhibition systems (BIS), which explain how an individual's motivational behavior influences their affective styles. Those with a heightened trait sensitivity to BAS are hypothesized to exhibit greater and avoid punishment; activation of this system is understood to promote goal-seeking behavior

(Coan & Allen, 2003). BIS, however, is hypothesized to be associated with greater , inhibitory behavior, and is sensitive to signals of punishment; suggesting that this system aids in avoiding the experience of painful or negative events (Balconi & Mazza, 2010).

Therefore, high BIS sensitivity is thought to be a predictive factor for developing an anxiety disorder as research shows that anxiety disorders promote significantly greater negative reactivity to emotional experience (Mennin et al., 2005). Empirical data suggest that greater BAS sensitivity (approach motivation and positive affectivity) should be accompanied by greater left

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY frontal activity, while increased BIS sensitivity (withdrawal motivation and negative affectivity) should be accompanied by greater right frontal activation (Coan & Allen, 2003). Both models are often used to describe behavioral tendencies of individuals with GAD. Therefore, based on past research and the predictions of these models, there is reason to believe that individuals with

GAD are prone to experiencing abnormal emotional perception and exhibiting abnormal frontal

EEG activity with greater relative right-sided frontal activity (i.e. relative less left alpha) when compared to left.

The Present Study

The available research on FAA and its relation to motivational and emotional tendencies provides reason to investigate whether or not individuals who exhibit significant symptoms of

GAD demonstrate different patterns in FAA (i.e. increased relative right frontal activity; relatively less right alpha) when compared to healthy individuals. Moreover, is this distinct FAA pattern shown during rest and when confronted with negative affective stimuli? It is important to note the value of the predictive power of FAA on emotional behavior, as it may be applied to improvements in diagnosis, evaluation, and treatment of mental disorders, such as GAD. While the models mentioned are not solely devoted to explaining GAD, research on anxiety confirms that GAD is indeed characterized by strong withdrawal- avoidance tendencies, intense emotional experiences, and impaired emotional perception (Mennin et al., 2005). Few EEG FAA studies solely focus on investigating GAD alone from other anxiety disorders, therefore this study may help contribute to this gap in research.

Considering these findings, it is hypothesized that individuals suffering from moderate to severe forms of GAD will exhibit greater relative right frontal activity; and thus relatively

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY diminished right alpha power, while consequently demonstrating increased sensitivity to negative emotional stimuli. This hypothesized pattern of activity is furthermore expected to be demonstrated during a resting state, free of any tasks or stimuli. These lines of inquiry were investigated via EEG experimentation as subjects were confronted with clips of the same neutral sentence that varied across trials among 3 modalities (A, V, AV), 3 emotions (happy, angry, ) and 2 emotional intensities (normal, strong). Subjects were to indicate which emotion was portrayed and how intense they perceived that emotion to be. This experiment also involved an investigation into resting FAA.

Materials and Methods

Participants

This study consisted of 60 male (n=10) and female (n=33) participants between the ages of 18 and 23; not all subjects wished to specify their gender. Subjects were first-year students at Tilburg University and were recruited via a university online program; students were awarded study credit for their participation. Prior to starting the experiment, subjects were provided with an information sheet of the experiment and were asked to read and sign an informed consent form.

Stimuli

Both the auditory and visual stimuli for this experiment were retrieved from the Ryerson

Audio-Visual Database of Emotional Speech and Song (RAVDESS) (Livingstone & Russo,

2018). Each of the expressions evoked in these videos are portrayed at two levels of emotional intensity (normal and strong). In the present study, only one of the available RAVDESS

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY statements was used (“Kids are talking by the door”) and only those files including happy, fear, and were included. Throughout the experiment, 3 emotions (happy, fear, anger) were presented in different modalities of: A-only (16bit, 48kHz .wav), AV (720p H.264, AAC

48kHz, .mp4), and V-only (no sound) (Livingstone & Russo, 2018). All visual stimuli were presented on the middle of the computer screen at a comfortable viewing distance of approximately 60 cm. The visual stimuli were presented in color at a resolution of 2560x1440 pixels (Livingstone & Russo, 2018). Audio was presented at a comfortable volume of about 65 dB via two speakers placed beside the monitor. Upon conclusion of all trials, a test of resting

FAA was conducted.

Design

This study implemented within-subject and between-subject measurements. Throughout the course of the experiment, subjects were connected to an EEG. The stimuli consisted of 24 speakers, 3 emotions (happy, angry, fear), and 3 modalities (A, V and AV), thus creating a total of 432 unique conditions. Each of the conditions were presented 2 times, for example: A-only, speaker 1, with high intensity fear stimulus. The 3 emotions presented in this experiment were displayed at 2 intensities (normal and strong). The purpose of including normal intensity expressions was to further investigate subtle differences in emotional (Livingstone &

Russo, 2018). Stimuli would appear on screen according to a unique combination (i.e.

A_Happy_Strong) after which the screen would change to a response page. The response page required participants to (1) rate the perceived intensity of the emotion on a 7 point Likert scale based on two extremes (normal or strong) and (2) to indicate their perception as to which emotion the stimuli elicited (happy, angry, fear).

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY

Procedure

Each participant was given an information sheet and an informed consent form prior to the start of the experiment. Participants were also asked to indicate their hand preference, gender, and medication if applicable (i.e. for ADHD, depression, anxiety, etc.). This experiment was conducted in a dimly lit, semi-noise canceling booth. This study was conducted using E-Prime

3.0 which was responsible for the presentation of stimuli and recording of responses.

Experiment

The experiment started with a short practice session of 6 randomly selected trials. The duration between the stimulus offset and response screen presentation was set at approximately

500 ms; the ITI was set at 1000 ms. The duration for stimulus offsets and response screen presentation and ITI was the same for both the practice block and real experiment. Upon the test leader starting the experiment and EEG recording, the subject was made aware of the start of the experiment on the screen. After the stimulus was presented, the response screen appeared and subjects were to first indicate which emotion the stimulus elicited followed by the perceived intensity on a 7 point scale. The real experiment consisted of 864 randomly-ordered trials divided over 9 blocks; the first 8 blocks had 100 trials while the last block had 64 trials. Subjects were given the option to take breaks in between each block. The final stage of the experiment involved a test of resting FAA. Instructions appeared on the center of the screen for the subject to direct their to the fixation cross. After 3 minutes, instructions informing the subject to close their eyes appeared; this also lasted 3 minutes. Once finished, the subject was told they successfully completed the experiment and were escorted out of the cabin, disconnected from the

EEG, and instructed on the questionnaire portion of the experiment.

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY

Questionnaire

The questionnaire used in this study is known as the GAD-7 scale. This scale is a 7-item self-report measure designed to identify symptoms of GAD present over the last two weeks

(Spitzer et al., 2006). For example, some symptoms on the GAD-7 list include ‘ nervous, anxious, or on edge’ and ‘having trouble relaxing’. Subjects were required to indicate the prevalence of the presented symptoms based on four ratings ranging from 0 (‘not at all’) to 3

(‘nearly every day’). The scores of each column from 0-3 were added to create a total score, which was evaluated by three predetermined cut-off points representing the severity of the GAD:

5 (‘mild’), 10 (‘moderate’), and 15 (‘severe’) (Spitzer et al., 2006).

EEG Recording & FAA Analysis

The EEG signals in this study were recorded from 64 electrodes using an elastic cap distributed evenly across the scalp. The distribution and location of the electrodes were based off of the standard implementation created by the Extended International 10-20 System (Jasper,

1958). The point of reference was derived from the two sensors placed on the left and right mastoid. One facial sensor was placed directly above the right eye on the brow bone and directly below the right eye at the bottom eyelid; these two sensors were responsible for measuring vertical eye movements. Additionally, two sensors were placed on the side of each eye, near the front of each temporal bone, in order to measure horizontal eye movements (Bastiaansen et al.,

2018). The EEG signals were sent into amplifiers and digitized at a sampling rate of 512 Hz.

The data were filtered offline to an average of left and right mastoids. The bandpass filters low cutoff was set at 1 Hz and high cutoff set at 40 Hz in order to extract the relevant ERP frequency band (Bastiaansen et al., 2018). In order to eliminate 50Hz interference, a notch filter of 50 Hz

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY was used. Data was segmented into 1500 ms epochs relative to auditory stimulus onset.

Segmenting the epochs at 1500 corresponds to the shortest duration of the presented auditory stimuli. Epochs with an amplitude change exceeding ±160 microV were rejected. All data were corrected for eye movements in order to avoid introducing unwanted artifacts from recorded eye movements (Gratton et al, 1983).

To measure FAA between subjects, EEG was transformed using fast Fourier transform in order to normalize the distributions, power values of the alpha band (8-12 Hz) were log transformed. To assess the relation between FAA and traits of generalized anxiety, an anterior- asymmetry index was computed (Harmon-Jones & Allen, 1997). Such an index is computed by subtracting the overall activity in the alpha frequency band at the left electrode from that of the right electrode. Recall that alpha power is inversely related to cortical activity, therefore, positive scores on the anterior-asymmetry index suggest more left-hemispheric activity (Thibodeau et al,

2006).

Analysis

Results

Due to drop-outs, incomplete measurements, and some technical difficulties (i.e. faulty battery, failed recording, etc.) only 47 out of the original 60 subject data were analyzed. The average score on the GAD-7 of those 47 subjects was 7.1 out of the possible total score of 15

(Table 1). The interpretation of GAD-7 scores were based off of three cut-off points representing the severity of the GAD: 5 (‘mild), 10 (‘moderate’), and 15 (‘severe’). The frequency of scores are illustrated in Figure 1.

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY

Table 1. Statistics GAD7_Score N Valid 47 Missing 0 Mean 7.0851 Median 7.0000 Mode 7.00 Std. Deviation 3.90557 Variance 15.253 Minimum 1.00 Maximum 15.00

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY

An additional grouping variable was made dividing GAD-7 scores into two groups based on the median score of 7. Group 1 (N=20) was all scores below the median and group 2 (N=20) was all scores above the median; all scores of 7 were not given a group (Missing=7). Results of a one-sample T-test, Table 2, suggests that the two groups significantly differ on GAD-7 scores.

Moreover, Table 3 shows a significant correlation, at the 0.01 level, between GAD-7 scores and group.

Table 2. One-Sample Test Test Value = 0 95% Interval Mean of the Difference t df Sig. (2-tailed) Difference Lower Upper Group 18.735 39 .000 1.50000 1.3381 1.6619 GAD-7 12.437 46 .000 7.08511 5.9384 8.2318

Table 3. Correlation among GAD-7 Scores and Group GAD7_Score Group GAD-7 Pearson Correlation 1 .895** Sig. (2-tailed) .000 N 47 40

Group Pearson Correlation .895** 1 Sig. (2-tailed) .000 N 40 40 **. Correlation is significant at the 0.01 level (2-tailed).

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY

Behavioral Intensity Scores

The behavioral intensity represents the gathered responses to perceived emotional intensity (Normal or Strong) across all modalities (AV, V, A), emotions (Happy, Angry, Fear), and intensities (Normal, Strong). For the present analysis only the auditory condition is considered as there is a need in emotion perception research to distinguish the neurological underpinnings between affective visual and auditory perception. Considering that most available research investigates the independent functions of visual emotional perception, it seems that there is a need to devote more exploration to affective prosody perception, especially when it relates to abnormal emotional perception.

Responses of behavioral intensity were measured via a 7-point Likert scale, with higher scores reflecting higher perceived emotional intensity. Considering a median split was conducted to make two GAD-7 score groups (group 1=low GAD; group 2=high GAD), the interaction between behavioral intensity and GAD-7 group was tested with a repeated measures general linear model ANOVA. The within-subject factors included 3 emotions (happy, angry, fear), and the 2 intensities (normal, strong). The between-subject factor for this ANOVA was the group variable. Results of the Multivariate Tests (Table 4), using Pillai’s Trace, revealed significant results for main effect of emotion: F(2,37)=44.605, p=1 x 10-3 and intensity: F(1,38)=665.046, p=1 x 10-3. A significant interaction effect was also found between emotion*intensity:

F(2, 37)= .764, p=1 x 10-3. These effects suggest that both the main effect of emotion and intensity, and their interaction effect, had a significant influence on the rating of behavioral intensity. Test of between subjects revealed no significant results (Table 5). No other significant results were found, which demonstrates that one’s membership to either GAD-7 group (group did not have an effect on behavioral intensity scores.

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY

Table 4. Multivariate Testsa Effect F Hypothesis df Error df Sig. emo Pillai's Trace 44.605b 2.000 37.000 .000 emo * Group Pillai's Trace .346b 2.000 37.000 .710 inten Pillai's Trace 665.046b 1.000 38.000 .000 inten * Group Pillai's Trace .209b 1.000 38.000 .650 emo * inten Pillai's Trace 59.740b 2.000 37.000 .000 emo * inten * Group Pillai's Trace 2.050b 2.000 37.000 .143

Table 5. Tests of Between-Subjects Effects Measure: Behavioral Intensity Score

Transformed Variable: Average

Source df Mean Square F Sig. Intercept 1 3625.871 1478.112 0 Group 1 0.34 0.139 0.712 Error 38 2.453

Two-tailed Pearson bivariate correlations were computed between subjects’ behavioral intensity response scores and their GAD-7 scores (Table 6). Results suggest no significant correlation exists between behavioral intensity response scores and GAD-7 scores.

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY

Table 6 Correlations among GAD-7 Scores and Behavioral Intensity Responses GAD- AHappy AAngry AAngry AFear AFear 7 AHappyNormal Strong Normal Strong Normal Strong GAD-7 Pearson 1 -.044 -.091 -.117 -.058 -.037 -.071 Correlation Sig. (2- .771 .544 .433 .699 .804 .637

tailed) N 47 47 47 47 47 47 47 **. Correlation is significant at the 0.01 level (2-tailed).

Behavioral Emotion Category Response

The average of correct proportion of responses per condition are illustrated in Figure 2.

For example, the variable ‘PropotionHappyResponse_AHappyNormal’ represents the proportion that subjects responded correctly with ‘happy’ when the stimulus was auditory only with normal intensity.

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY

In order to determine if the proportion of correct behavioral-emotion responses per condition was influenced by GAD-7 group, a repeated measures general linear model ANOVA was conducted. The within-subject factors included 3 emotions (happy, angry, fear), and the 2 intensities (normal, strong). The between-subject factor for this ANOVA was the group variable.

Table 7 shows the results of the Multivariate Tests, using Pillai’s Trace. A significant main effect was found for emotion: F(2,37)=83.481, p=1 x 10-3 and intensity: F(1,38)=15.128, p=1 x 10-3.

These main effects suggest that, overall, significant differences of proportion of correct responses exist based on emotion and intensity. The main effect group was not significant, suggesting that one’s membership in either GAD-7 group did not influence proportion of correct behavioral-emotion responses (Table 8). A significant interaction was found between the factor emotion and intensity: F(2,37)=44.925, p=1 x 10-3. This effect implies a significant difference of proportion of correct responses between particular emotion-intensity combinations.

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY

Table 7 Multivariate Testsa Hypothesis Effect F df Error df Sig. emo Pillai's Trace 83.481b 2.000 37.000 .000 emo * Group Pillai's Trace .025b 2.000 37.000 .975 inten Pillai's Trace 15.128b 1.000 38.000 .000 inten * Group Pillai's Trace 2.751b 1.000 38.000 .105 emo * inten Pillai's Trace 44.925b 2.000 37.000 .000 emo * inten * Group Pillai's Trace .305b 2.000 37.000 .739

Table 8 Tests of Between-Subjects Effects Measure: Behavioral Emotion Category Response

Transformed Variable: Average Source F df Sig. Intercept 23630.124 1 .000 Group .268 1 .608 Error 1

The significant main effect of emotion suggests there is an overall significant difference in proportion correct based on emotion. In order to determine which specific emotions elicited the effect, a post-hoc analysis was conducted. Table 9 shows the results of the Pairwise comparisons with a Bonferroni correction to keep the Type I error at 5% overall; this analysis is indicative of which pairings of emotions are significantly different from one another. Results indicate, for proportion of correct behavioral-emotion responses, there is a significant pairwise difference between happy, angry, and fear. This demonstrates that each emotion had a

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY significantly different effect on subjects’ proportion of correct responses. For example, proportion of correct responses reduced by 0.174 between emotion angry and happy, and decreased by 0.126 between fear and happy, suggesting that overall, participants did better in identifying correct happy stimuli in the auditory only condition.

Table 9 Pairwise Comparisons Measure: Behavioral Emotion Category Response

Mean 95% Confidence Interval for (J) Difference Differenceb (I) emo emo (I-J) Std. Error Sig.b Lower Bound Upper Bound 1 2 -.174* .014 .000 -.210 -.138 3 -.126* .016 .000 -.166 -.086 2 1 .174* .014 .000 .138 .210 3 .048* .008 .000 .027 .068 3 1 .126* .016 .000 .086 .166 2 -.048* .008 .000 -.068 -.027 Based on estimated marginal means *. The mean difference is significant at the .05 level. b. Adjustment for multiple comparisons: Bonferroni.

The significant interaction for emotion*intensity was further investigated via simple effects test (Table 10). Table 10 displays the breakdown of the means for the different emotion- intensity combinations. Results indicate that, for the auditory only condition, proportion of correct emotion category responses was highest for emotion 2 (angry) especially at intensity 2

(strong), followed by fear, then happy. Therefore, across all subjects, the condition which elicited

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY the most correct responses was that of AAngry_Strong, The condition which elicited the most incorrect responses was AHappy_Normal.

Table 10 Emo * Inten Measure: Behavioral Emotion Category Response 95% Confidence Interval emo inten Mean Std. Error Lower Bound Upper Bound 1 1 .855 .014 .826 .883 2 .716 .015 .685 .747 2 1 .920 .009 .902 .937 2 .973 .004 .965 .982 3 1 .893 .008 .877 .909 2 .918 .007 .905 .931

FAA & Experimental Data

The interaction between GAD-7 score and FAA during the perception of emotional utterances across conditions was tested with a repeated measures general linear model ANOVA.

Prior to the analysis, the natural log-transformed alpha power in the left and right hemispheres were calculated in order to determine if FAA was present. Based on their frontal region location on the EEG cap, the following corresponding electrodes were used in the calculation: FP2_FP1,

F8_F7, F6_F5, F4_F3, F2_F1, FT8_FT7, FC6_FC5, FC4_FC3, and FC2_FC1. Figure 3 depicts the electrode asymmetries per experimental conditions with positive values indicating relative left frontal activity, and therefore less left alpha power, compared to right. Negative values indicate right frontal activity, and thus relatively less right alpha power, compared to left.

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY

Based on the figure, it is clear that across subjects FP2_FP1_AAngryNormal shows the most left frontal activity, while FT8_FT7_AHappyStrong shows the most right frontal activity.

Figure 3

The within-subject factors for the ANOVA included the 9 electrodes, 3 emotions (happy, angry, fear), and 2 intensities (normal, strong). The between subject variable was the GAD-7 score group variable. Table 11 displays the results of the Multivariate tests using Pillai’s Trace which revealed a significant main effect of electrode: F(8,31)= 2.408, p=<.05. Tests of between subjects revealed no significant effects (Table 12). Considering the main effect of electrode is not of interest in the current study, no further investigation of the effect was conducted.

Therefore, results indicate that no significant differences in FAA exist between GAD-7 score during the perception of emotional utterances across conditions.

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY

Table 11 Multivariate Testsa Hypothesis Error Effect F df df Sig. elec Pillai's Trace 2.408b 8.000 31.000 .038 elec * Group Pillai's Trace 1.548b 8.000 31.000 .181 emo Pillai's Trace .208b 2.000 37.000 .813 emo * Group Pillai's Trace .755b 2.000 37.000 .477 inten Pillai's Trace .327b 1.000 38.000 .571 inten * Group Pillai's Trace 1.863b 1.000 38.000 .180 elect * emo Pillai's Trace .770b 16.000 23.000 .701 elec * emo * Group Pillai's Trace .748b 16.000 23.000 .722 elec * inten Pillai's Trace 1.527b 8.000 31.000 .188 elec * inten * Group Pillai's Trace 1.442b 8.000 31.000 .219 emo * inten Pillai's Trace .985b 2.000 37.000 .383 emo * inten * Group Pillai's Trace 1.499b 2.000 37.000 .237 elec * emo * inten Pillai's Trace 1.989b 16.000 23.000 .065 elec * emo * inten * Pillai's Trace 1.613b 16.000 23.000 .144 Group

Table 12. Tests of Between-Subjects Effects

Measure: FAA Transformed Variable: Average

Source F df Sig. Intercept .023 1 .881 Group .053 1 .819 Error 38

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY

In an attempt to investigate whether or not there was significant change in FAA across different conditions, a one-sample t-test against zero was conducted on these sensors across the auditory modality, 3 emotions, and 2 intensities. Significant results (Table 13) include:

FP2_FP1_AAngryNormal: t(46) = 4.262, p=1 x 10- 3; FP2_FP1_AAngryStrong: t(46)=2.968, p= 5 x 10- 3; FP2_FP1_AHappyNormal: t(46)= 3.317, p=2 x 10- 3; FP2_FP1_AHappyStrong: t(46)=3.987, p=.1 x 10- 3; FP2_FP1_AFearNormal:t(46)=2.991, p=4 x 10- 3; and

FP2_FP1_AFearStrong: t(46)=3.115, p=3 x 10- 3.

Table 13 One-Sample Test Test Value = 0 95% Confidence Interval Sig. (2- Mean of the Difference t df tailed) Difference Lower Upper FP2_FP1_AAngryNormal 4.262 46 .000 .05441 .0287 .0801 FP2_FP1_AHappyNormal 3.317 46 .002 .04618 .0182 .0742 FP2_FP1_AFearNormal 2.991 46 .004 .04094 .0134 .0685 FP2_FP1_AAngryStrong 2.968 46 .005 .04161 .0134 .0698 FP2_FP1_AHappyStrong 3.987 46 .000 .05049 .0250 .0760 FP2_FP1_AFearStrong 3.115 46 .003 .05199 .0184 .0856

Figure 4 represents the electrode asymmetries per experimental condition of these significant electrodes. Based on the figure it is evident that all of the significant electrodes show positive values, indicating more left frontal activity (i.e. less left alpha power) when compared to right.

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY

Figure 4

To further analyze these significant results, a two-tailed Pearson bivariate correlation was conducted between GAD-7 scores and FAA at the electrodes that showed an overall significant

FAA; results show no significant correlations (Table 14). This suggests that while these electrodes showed significant FAA per condition, no significant correlations exist between

GAD-7 scores and FAA.

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY

Table 14 Correlations FP2_ FP2_F FP2_ FP2_ FP2_ FP2_ FP1_ P1_A FP1_ FP1_ FP1_ FP1_ AAn Happy AFea AAn AHa AFea GAD gryN Norm rNor grySt ppySt rStro

-7 ormal al mal rong rong ng GAD Pearson 1 -.048 .065 .082 .175 .043 .043 -7 Correlation Sig. (2- .748 .662 .583 .238 .773 .776 tailed) N 47 47 47 47 47 47 47 **. Correlation is significant at the 0.01 level (2-tailed).

Resting EEG Data

These data points show the average resting alpha power of each sensor for each participant across three minutes of recording (eyes closed). In order to determine if any FAA was present, the natural log-transformed alpha power in the left and right hemispheres were calculated using the following corresponding electrodes: FP2_FP1, AF8_AF7, AF4_AF3,

F8_F7, F6_F5, F4_F3, F2_F1, FT8_FT7, FC6_FC5, FC4_FC3, and FC222_FC1. A repeated measures general linear model ANOVA was conducted to investigate if there was a significant difference in resting FAA among GAD-7 groups. The within-subject factors included those electrodes while the between-subject factor was the group variable. The results of the

Multivariate Tests (Table 15), using Pillai’s Trace, revealed no significant results, demonstrating that resting FAA did not significantly differ between GAD-7 groups.

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY

Table 15 Multivariate Testsa Hypothesis Effect F df Error df Sig. Elec Pillai's Trace 1.919b 10.000 29.000 .083 Elec * Group Pillai's Trace .716b 10.000 29.000 .703

Two-tailed Pearson bivariate correlations were then computed between the given resting frontal EEG asymmetry natural logs and the GAD-7 scores. As shown in Table 16, individual

GAD-7 scores shared no significant correlations with resting FAA.

Table 16 Correlations GA D- F6_ F4_ F8_ F2_ FP2_ FT8_ FC6_ FC4_ FC2_ AF8_ AF4_ 7 F5_ F3_ F7_ F1_ FP1_ FT7_ FC5_ FC3_ FC1_ AF7_ AF3_ GA Pearso 1 -.08 -.04 -.11 -.13 .181 -.080 -.087 .122 -.023 .023 .174 D- n 3 4 6 8 7 Correl ation Sig.(2- .580 .772 .436 .356 .224 .594 .563 .415 .880 .879 .243 tailed) N 47 47 47 47 47 47 47 47 47 47 47 47 *. Correlation is significant at the 0.05 level (2-tailed). **. Correlation is significant at the 0.01 level (2-tailed).

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY

Discussion

This study was comprised of an EEG experiment which investigated aspects of emotional perception in generalized anxiety disorder while evaluating FAA. Results indicated that subjects’ level of generalized anxiety, based on the GAD-7, did not have a significant effect on the recognition or perceived intensity of emotions. Therefore, no differences in emotional perception were found between those with high and low scores of GAD. It was hypothesized that those who had higher GAD-7 scores would, for example, rate normal angry stimuli as more intense based on predictions from the approach-withdrawal and BIS/BAS models. These findings are not consistent with past research into GAD which claim that those with higher GAD levels experience significantly more difficulty in the identification and description of emotions when compared to healthy control groups (Demenescu et al., 2011; Mennin et al., 2005; Turk et al.,

2005). This inconsistency may be explained by the differences in stimuli between the current study and past studies regarding GAD and emotional perception. For example, Sandra &

Newman (2010) provoked emotional states via guided instructions (i.e. “think about your most worrisome topic and worry about it as intensely as you can”) followed by emotional recognition and rating tasks. Mennin et al., (2005) also tested emotional perception through inducing a certain mood via instructions and specific emotion-eliciting prior to measuring emotional perception. Therefore, the results of the current study may reflect that GAD is less sensitive to negative emotional tones of neutral sentences when compared to specific emotion-eliciting utterances or scenarios.

Moreover, across all GAD-7 scores, no differences in FAA at rest or during the task were found; suggesting that generalized anxiety does not have a significant effect on FAA. Based on approach-withdrawal and BIS/BAS research, those with higher levels of GAD should have

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY demonstrated increased relative right frontal activity and thus less right alpha power when compared to left (Van Der Vinne et al., 2017; Coan & Allen, 2003). It should be noted, however, that the analyzed electrode asymmetries per condition (Figure 3) showed that across subjects

FP2_FP1_AAngryNormal corresponded with the most left frontal activity while

FT8_FT7_AHappyStrong showed the most right frontal activity. This is not consistent with the multiple studies that have found approach and positive affectivity corresponds to increased relative left frontal activity while withdrawal and negative affectivity correspond with increased relative right frontal activity (Van Der Vinne et al., 2017; Hagemann et al., 2002; Coan & Allen,

2003; Balconi & Mazza, 2010; Wheeler et al., 1993). An explanation for this discrepancy could again be the differences in stimuli between the current study and past research. For example,

Wheeler et al., (1993) used videos to investigate FAA and affective style. Recall that most research regarding emotional perception has primarily used visual stimuli and found ‘visual dominance in the perception of affective expressions’ (Collignon et al., 2008). Therefore, it is difficult to compare the results of the current study with past research as most investigations into emotional perception have not solely implemented auditory-only stimuli. Moreover, it is important to note that available research does not provide independent investigations of GAD and FAA but rather focuses on approach-withdrawal and behavioral inhibition-activation tendencies that are presented in various anxiety disorders. Therefore, independent investigations of different anxiety disorders are needed to distinguish distinct differences in FAA and thus emotional perception.

Another limitation in the current research is the participant profile as subjects used in this experiment were limited to university students which limits the generalizability to the greater societal setting due to lifestyle, age, education, etc. Furthermore, subjects were diagnosed via

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY self-report without additional structured interviews, as is standard in clinical settings when determining an official psychiatric diagnosis. While participants in this study did take additional questionnaires regarding other psychiatric disorders, this was not considered or cross-analyzed in the present analysis. Past research, such as Mennin et al., (2005) implemented a battery of tests for different types of and psychopathologies in order to further the validity of the GAD self-report. Had such considerations taken place, perhaps it would have been helpful in ruling out any influential commonalities and or comorbidities of other psychiatric disorders and GAD.

Furthermore Mennin et al., (2005) also ran their experiment on out-patients who have been undergoing treatment for GAD which may also contribute to the differences in results when considering symptom severity, medication, influence of therapy, etc.

Results from the present study suggest that no differences in FAA exist between individuals with significant symptoms of GAD and those without. More extensive research regarding the relationship between emotion dysregulation and specific disorders is needed.

Furthermore, there is a necessity to create a distinction between perception of neutral emotional stimuli and emotion-specific stimuli. Moreover, further studies investigating large scale clinical samples of GAD, and other psychopathologies, alongside a community control sample would be useful in identifying disorder-specific neurological underpinnings. More studies investigating emotional perception using only auditory stimuli are needed to further investigate differences in affective visual and auditory perception among psychopathologies. When considering the evidence provided by related studies on the current topic, there is reason to believe that such advancements in research would further improve our understanding of such psychopathologies and their prevention, diagnosis, and treatment.

GAD & AUDITORY EMOTION PERCEPTION: AN EEG FAA STUDY

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