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Affective responses to EEG preparation and their link to resting anterior EEG asymmetry
Personality and Individual Differences 32 (2002) 167±174
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Aective responses to EEG preparation and their link to resting anterior EEG asymmetry Ginette C. Blackhart *, John P. Kline, Keith F. Donohue, Steven D. LaRowe, Thomas E. Joiner Department of Psychology, Florida State University, Tallahassee, FL 32306, USA Received 18 September 2000; accepted 29 December 2000
Abstract Previous research relating anterior asymmetry in the electroencephalogram (EEG) to emotional states has not taken the aective context of the testing environment into account. This may be an important consideration, as the preparation procedures themselves are somewhat aversive. The purpose of this study was to assess whether self-reported mood state before and/or after EEG cap preparation was associated with EEG asymmetry. Mood state was assessed with the self-assessment manikin before and after the application of the electrode cap. Men and women showed a shift toward a more negative mood state postpreparation. Negative mood post-preparation, but not pre-preparation, predicted relative right frontal activation in men. In contrast, negative mood post-preparation, but not pre-preparation, predicted relative left frontal activation in women. Results are discussed as they relate to gender dierences in interpersonal engagement. # 2001 Elsevier Science Ltd. All rights reserved. Keywords: EEG; Gender dierences; EEG asymmetry
1. Introduction The experience of positive, approach-related behavior has been associated with left frontal and anterior temporal electroencephalographic (EEG) activation1, while the experience of negative, withdrawal-related behavior has been associated with right frontal and anterior temporal EEG activation (Ahern & Schwartz, 1985; Davidson, 1995; Heller, 1990; Tomarken, Davidson, & * Corresponding author. Tel.: +1-850-644-2040; fax: +1-850-644-7739. E-mail address: [email protected] (G.C. Blackhart). 1 Power in the alpha band is generally interpreted as an inverse index of brain activation (Davidson, 1995). For the rest of this paper, we will use ``activation'' to refer to a decrease in power in the alpha (e.g. 8±13 Hz) band. 0191-8869/01/$ - see front matter # 2001 Elsevier Science Ltd. All rights reserved. PII: S0191-8869(01)00015-0
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Henriques, 1990). Several lines of research converge to support this model. Victims of right and left frontal strokes show distinct aective changes (for a review, see Liotti & Tucker, 1995). Individuals with left frontal lesions due to stroke show more depressive and withdrawal behaviors, while people with right frontal lesions show more approach behavior, which can result in jovial mood, manic behavior, or pseudopsychopathy (Davidson, 1995; Kolb & Whishaw, 1996). Substantial research has documented the trait properties of the frontal EEG asymmetry (see Davidson, 1995, for a review), and a prediction from this literature is that left frontal active individuals should be more responsive to positive stimuli, whereas right frontal active individuals should be more responsive to negative stimuli. Davidson and Fox (1989) recorded baseline EEG measures from 10-month-old infants. Infants who were right frontally active during baseline later cried when separated from their mothers, while infants who were left frontally active did not cry in response to maternal separation. Tomarken et al. (1990) reported similar results in a study of adult women in response to emotionally salient ®lm clips. Women who showed increased right frontal activation at baseline were more likely to report a negative aective response to the aversive ®lm clips and a more globally negative mood. These results suggest that an individual's resting relative right frontal activation is linked to a lowered threshold for negative aective reactions to aversive stimuli (Tomarken et al., 1990). Similarly, relative left-frontal activation has been hypothesized to relate to a more global predisposition to experience positive mood. Consistent with this hypothesis, Tomarken, Davidson, Wheeler and Doss (1992) reported that women who demonstrated relative left anterior EEG activation reported increased positive aect and decreased negative aect compared with women who showed relative right anterior EEG activation. Jacobs and Snyder (1996) have reported a similar phenomenon in men. Furthermore, depressed individuals tend to exhibit decreased left frontal activation or increased right frontal activation (Gotlib, Ranganath, & Rosenfeld, 1998; Henriques & Davidson, 1990, 1991; Schaer, Davidson, & Saron, 1983). This phenomenon occurs during acute episodes of depression, but has also been observed in previously depressed individuals who are in remission (Allen, Iacono, Depue, & Arbisi, 1993; Henriques & Davidson, 1990), which again suggests that relative activation is related to a state-independent dispositional mood diathesis. Similarly, increased left frontal activation has been related to putative indicators of decreased vulnerability for depression (Harmon-Jones & Allen, 1997; Kline, Allen, & Schwartz, 1998; Kline, Blackhart, & Schwartz, 1999; Sutton & Davidson, 1997; Tomarken & Davidson, 1994). While EEG asymmetry has trait components, other research has demonstrated that frontal asymmetry responds to aective manipulations. For example, Ahern and Schwartz (1985) measured EEG in women who had just completed a task that was designed to elicit positive and negative aect. They reported that positive aect correlated with left frontal EEG activation, while negative aect correlated with right frontal activation. Similarly, Wheeler, Davidson, and Tomarken (1993) elicited positive and negative aect with emotional ®lm clips and found similar results in relative EEG activation. Related research suggests the association of left frontal activation with approach motivation, and the association of right frontal activation with withdrawal motivation (Davidson, 1992; Harmon-Jones & Allen, 1997; Sutton & Davidson, 1997). Though subjective mood at the time of testing has typically not correlated with frontal asymmetry (Tomarken & Davidson, 1994; Tomarken et al., 1990), the aect manipulations in these studies have used post-EEG preparation measures as their mood baseline (e.g. Tomarken et al., 1990). This assessment of baseline mood comes after the EEG preparation procedures, which
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may be somewhat unpleasant. The procedures include the ®tting of a tight cap to participants' heads, the abrasion of their scalps with a blunt probe, and the application of cold, wet electrode gel in the hair. The procedure usually requires 30 min to complete. Not surprisingly, participants appear to vary in their responses to this. Informal observations have some participants stoically enduring the procedure without a complaint, while some wince noticeably. Furthermore, other participants ask questions about the procedures, appear to be amused, and engage in conversations with the experimenters. The purpose of this study was to determine whether subjective mood correlates with frontal asymmetry after taking the EEG preparation into account. We were interested in whether: (1) the application of the EEG cap would produce a relative decrease in positive aect; and (2) whether the time of baseline mood assessment (i.e. pre or post-preparation) made a dierence in whether or not baseline mood predicted frontal asymmetry. As an additional exploratory measure, we assessed gender dierences in the relation between baseline mood and resting anterior asymmetry. 2. Method 2.1. Participants Thirty-six men and 41 women (all right handed) ranging in age from 16 to 39 (mean age=20.5, S.D.=3.70) volunteered to participate in the study. Participants were undergraduates in an Introduction to Psychology class, and received course credit for their participation. All men and women in the study interacted with an equal number of female and male experimenters. 2.2. Questionnaire administration and scoring Participants signed a consent form and completed questionnaires prior to EEG recording. Handedness was assessed with the Edinburgh Handedness Inventory (Old®eld, 1971). The selfassessment manikin (SAM) was used to measure pleasant mood (on the valence dimension) both before and immediately after participants were connected to the EEG cap. The SAM is a nonverbal method for quickly assessing valence, arousal, and dominance associated with an individual's emotional reaction to an event. It is an adaptation of the verbal semantic dierential scale developed by Mehrabian and Russell (1974), that measures emotions on three dimensions: pleasure-displeasure, arousal-nonarousal, and dominance-submissiveness. Mehrabian and Russell's semantic dierential scales showed sucient reliability, with 0.94 for pleasure-displeasure (Russell & Mehrabian, 1977). SAM ratings are highly related to the Mehrabian and Russell's semantic dierential scale, with a correlation of 0.97 for the pleasure-displeasure dimension (Bradley & Lang, 1994). Each scale ranges from 1 to 9, and on the pleasure-displeasure scale 1 indicates an unpleasant mood, 9 indicates a very pleasant mood, and 5 indicates a neutral mood. This scale corresponds to pictures of the SAM ®gure that range from smiling and happy to frowning and unhappy (Morris, 1995). Assessments with the SAM may elicit more consistent judgments concerning emotional reactions because the SAM ®gures are human-like (Bradley & Lang, 1994). For these reasons, the SAM pleasure-displeasure scale was judged to be a good measure of subjective pleasant mood both before and after EEG preparations.
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2.3. EEG recording and quanti®cation Resting EEG was recorded with a stretch lycra electrode cap with tin electrodes (Electrocap International, Eaton, Ohio) from a standard International 10-20 system of 19 channels referenced to linked ears. Data collection and reduction were accomplished with Neurolex software and a Neurosearch 24 data acquisition unit. Electrode gel was applied to each electrode, and the scalp at each site was gently abraded until impedances were below 10 k . Homologous leads (EEG and auricular leads) were within 1 k of each other. EEG records were visually examined for artifact, and epochs containing bioelectric artifact greater than 75 microvolts in any channel were rejected. Data were digitized on-line at 256 Hz (60 Hz notch ®lter enabled) during six 60 s periods, three with eyes open and three with eyes closed. Highpass ®lters were set at 2 Hz, and had a rollo of 6 dB per octave (®rst order), and lowpass ®lters were set at 64 Hz and had a rollo of 48 dB per octave (eighth order). Non-overlapping, artifact-free epochs of 256 samples (i.e. 1-s epochs) were extracted through a Hanning window and submitted to Fast Fourier Transform. Power was extracted in 1 Hz bins, which were combined into spectral bands. Average alpha (8±13 Hz) power (microvolts squared) was natural log transformed for normalization. A natural log transformation technique was used to normalize the distributions of power values, as these distributions tend to be positively skewed. This is consistent with the recommendations of Davidson, Ekman, Saron, Senulis, and Freisen (1990). Because alpha power has been found to be inversely related to the activation of the corresponding region of the brain, researchers have contended that anterior alpha asymmetry measurements re¯ect relative dierences in activity between the left and right hemispheres (Davidson, 1995). The alpha activity in the left side is subtracted from the alpha activity in the right side, and higher values indicate greater left-sided activation. Asymmetry scores were computed (log[right]-log[left]) for Fp2-Fp1, F4-F3, F8-F7, T4-T3, T6-T5, C4-C3, P4P3, and O2-O1. 2.4. Design and analysis In order to assess whether the preparation procedure was associated with a decrease in positive mood from pre to post-preparation, ANOVA was conducted for the pleasure dimension on the SAM from pre to post EEG cap preparation. General linear model analyses were conducted in order to assess whether T1 and/or T2 mood valence predicted ASYM for men and women. Time 1 mood (pre-preparation; T1), time 2 mood (post-preparation; T2), sex, T1SEX, and T2SEX were entered into the analysis. Follow-up analyses were conducted separately for women and men. 3. Results ANOVA revealed there was a signi®cant main eect for time F(1, 76)=13.49, P<0.001, where participants rated themselves as feeling signi®cantly less pleasant from T1 (M=5.91, S.D.=1.39) to T2 (M=5.40, S.D.=1.44). Zero order correlations show that for the entire sample, a signi®cant correlation was found between T1 and T2 mood. For men, a signi®cant correlation was found between T1 and T2
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mood. For women, signi®cant correlations were found between ASYM at F4-F3 and T2 mood, between ASYM at F8-F7 and T2 mood, and between T1 and T2 mood (Table 1). 3.1. Regression analyses There was a signi®cant multivariate interaction between T2 mood valence and sex F(8, 64)=2.72, P<0.02. The interaction of T1 mood valence and sex did not signi®cantly predict asymmetry F(8, 64)=1.06, P<0.40. There were signi®cant univariate eects at F4±F3 t(71)= 3.47, P<0.001 and at F8±F7 t(71)= 3.57, P<0.001, where the interaction of T2 mood valence and sex signi®cantly predicted asymmetry. No other signi®cant univariate eects were found at Fp2±Fp1, C4±C3, P4±P3, T4±T3, T6±T5, or O2±O1. In the follow-up analyses for men, T1 and T2 valence accounted for 11% of the variance in mid-frontal asymmetry (F4±F3) scores F(2, 33)=2.13, P<0.14, and 12% of the variance in lateral frontal asymmetry (F8±F7) scores F(2, 33)=2.31, P<0.12. The partial correlation of T2 mood with T1 mood partialed out signi®cantly predicted ASYM at F4±F3 =0.45, t(33)=2.06, P<0.05 and at F8±F7 =0.45, t(33)=2.06, P<0.05. Mood at T1 did not signi®cantly predict ASYM at F4±F3 (P<0.23) or at F8±F7 (P<0.38). T2 negative mood valence was associated with relative right frontal activation in men. In the follow-up analyses for women, T1 and T2 valence accounted for 25% of the variance in mid-frontal asymmetry, F(2, 38)=6.42, P<0.005, and 24% of the variance in lateral frontal asymmetry, F(2,38)=5.92, P<0.01. The partial correlation of T2 mood with T1 mood partialed out signi®cantly predicted ASYM at F4±F3 = 0.51, t(38)= 2.93, P<0.01 and at F8±F7 = 0.56, t(38)=±3.19, P<0.01. Mood at T1 did not predict ASYM at F4±F3 (P<0.88) or at F8±F7 (P<0.42). T2 negative mood valence was associated with relative left frontal activation in women.
Table 1 Zero order correlations between assymmetry (ASYM), Time 1 (T1) mood, and Time 2 (T2) mood ASYM Entire sample ASYM T1 Valence T2 Valence Men ASYM T1 Valence T2 Valence Women ASYM T1 Valence T2 Valence *P< 0.05
T1 valence
T2 valence
±
0.11 ±
0.08 0.64* ±
±
0.02 ±
0.27 0.66* ±
±
0.29 ±
0.50* 0.59* ±
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4. Discussion Overall, the EEG cap application appeared to lead to a less positive mood. Given the nature and duration of the procedure, this is hardly surprising. Since psychophysiological measurements are often used for subtle assessments of emotional functioning, this result underscores the importance of taking the measurement context into account when interpreting EEG asymmetry/ mood relations. The measures of mood most proximate to the EEG recordings were associated with asymmetry when the results of pre-cap preparation mood ratings were statistically controlled. Pre-cap preparation mood measures were unrelated to EEG asymmetry. This suggests that the mood/EEG relations that we described in this study were very much state-speci®c. The gender dierence obtained in this study was unexpected, and is dicult to interpret. While male participants met predictions by showing a positive association, albeit a weak one, between pleasantness and asymmetry, the result was opposite and more robust for women. Not only were these results for female participants contrary to the predictions of the study, but were also inconsistent with other research that assessed female participants' reactions to negative stimuli (Davidson & Fox, 1989; Tomarken et al. 1990). In this context, the nature of our study's negative stimulus Ð the preparation procedure Ð is important to consider. The procedure, although certainly mildly aversive, also includes a buering interpersonal in¯uence; namely, the experimenter, whose presence and supportive words may be reassuring to participants, especially to particular participants (e.g. women). Importantly, negative stimuli used in other studies, such as an aversive ®lm clip, probably do not contain this buering in¯uence. We suggest that this interpersonal buer had two eects on women, more so than on men: (1) women were more interpersonally engaged with the experimenter than were men (and engagement has been shown to contribute to relative left frontal activation); and (2) in part because women were more interpersonally engaged and thus felt more supported, they were more emotionally expressive than men about the context (and here, the context of the preparation was mildly aversive, perhaps encouraging expression of negative emotion among women). Women who became more engaged with the entire context, including with the experimenter, may have been more likely to display left frontal activation and more likely to vent emotions about the context, producing the association between left frontal activation and negative mood in women. By contrast, men may have been less aected by or less responsive to the buering eects of the experimenter, and thus may have experienced the preparation procedure as uniformly negative, much as if they had been viewing an aversive ®lm clip; and, in our regression analyses, ®ndings from men mirrored ®ndings from studies using aversive ®lm clips and other similar stimuli Ð right frontal activation was associated with negative mood among men. We emphasize that this is a speculative explanation, in need of empirical scrutiny. However, past research lends some credence to elements of this explanation. For example, there is some indication that women are more ``engageable'' than men, in that they endorse more aliative needs than men (e.g. Cheng, 1999), and appear to be more protected by social support and to value it more highly than men (e.g. Barker, Morrow, & Mitteness, 1998; Schraedley, Gotlib, & Hayward, 1999). Moreover, there is some indication that women, more so than men, may constructively cope with adversity by expressing negative emotions (Stanton, Dano-Burg, Cameron, & Ellis, 1994).
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In sum, we predicted that left frontally active participants in this study would ®nd the process of EEG cap application less aversive than those who were right frontally active. This result was obtained for men, but women showed the opposite result. Future research may wish to pay attention to contextual and preference factors that might mediate such gender dierences in anterior asymmetry/mood relationships, and may also wish to focus on gender dierences in interpersonal engagement as it relates to anterior asymmetry. Future EEG research also needs to pay careful attention to the fact that psychophysiological research, strictly speaking, never truly measures traits per se, but only those traits as they interact with our experimental protocols. This leaves the possibility of trait/state interactions in all of our data, even when experiments are designed to speci®cally measure traits. We assume that by holding our procedures constant across participants, all participants will respond similarly to the procedures that we do not typically think of as manipulations (e.g. EEG preparation, interaction with the experimenter, etc.). Therefore, we need to develop some way to better measure basal trait EEG. One possibility is to introduce a relaxation phase to the participants after the EEG cap preparation in an attempt to observe stabilized trait anterior asymmetry. This way a basal ratio can be obtained dynamically prior to a speci®c experimental manipulation. Another possibility is to use a less invasive procedure, such as a geodesic sensor net (Electrical Geodesics Incorporated, Eugene, OR). This system allows for the placement of electrolyte-impregnated sponges on the participant's scalp, and does not necessitate extensive scalp abrasion. These two methods may allow for less procedural reactivity, allowing for a better estimate of basal, trait asymmetry. References Ahern, G. L., & Schwartz, G. E. (1985). Dierential lateralization for positive and negative emotion in the human brain: EEG spectral analysis. Neuropsychologia, 23, 745±756. Allen, J. J., Iacono, W. G., Depue, R. A., & Arbisi, P. (1993). Regional electroencephalographic asymmetries in bipolar seasonal aective disorder before and after exposure to bright light. Biological Psychiatry, 33, 642±646. Barker, J. C., Morrow, J., & Mitteness, L. S. (1998). Gender, informal social support networks, and elderly urban African Americans. Journal of Aging Studies, 12, 199±222. Bradley, M. M., & Lang, P. J. (1994). Measuring emotion: the self-assessment manikin and the semantic dierential. Journal of Behavioral Therapy and Experimental Psychiatry, 25, 49±59. Cheng, C. (1999). Gender-role dierences in susceptibility to the in¯uence of support availability on depression. Journal of Personality, 67, 439±467. Davidson, R. J. (1995). Cerebral asymmetry, emotion, and aective style. In R. J. Davidson, & K. Hugdahl, Brain asymmetry (pp. 361±387). Cambridge: MIT. Davidson, R. J. (1992). Anterior cerebral asymmetry and the nature of emotion. Brain and Cognition, 20, 125±151. Davidson, R. J., Ekman, P., Saron, C., Senulis, J., & Freisen, W. V. (1990). Approach/withdrawal and cerebral asymmetry: emotional expression and brain physiology, I. Journal of Personality and Social Psychology, 58, 330±341. Davidson, R. J., & Fox, N. A. (1989). Frontal brain asymmetry predicts infants' response to maternal separation. Journal of Abnormal Psychology, 98, 127±131. Gotlib, I. H., Ranganath, C., & Rosenfeld, J. P. (1998). Frontal EEG alpha asymmetry, depression, and cognitive functioning. Cognition and Emotion, 12, 449±478. Harmon-Jones, E., & Allen, J. J. B. (1997). Behavioral activation sensitivity and resting frontal EEG asymmetry: covariation of putative indicators related to risk for mood disorders. Journal of Abnormal Psychology, 106, 159±163. Heller, W. (1990). The neuropsychology of emotion: Developmental patterns and implications for psychopathology. In N. Stein, B. L. Leventhal, & T. Trabasso, Psychological and biological approaches to emotion (pp. 167±211). Hills ale, NJ: Erlbaum.
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Henriques, J. B., & Davidson, R. J. (1991). Left frontal hypoactivation in depression. Journal of Abnormal Psychology, 100, 535±545. Henriques, J. B., & Davidson, R. J. (1990). Regional brain electrical asymmetries discriminate between previously depressed and healthy control subjects. Journal of Abnormal Psychology, 99, 22±33. Jacobs, G. D., & Snyder, D. (1996). Frontal brain asymmetry predicts aective style in men. Behavioral Neuroscience, 110(1), 3±6. Kline, J. P., Allen, J. J. B., & Schwartz, G. E. (1998). Is left frontal brain activation in defensiveness gender speci®c?. Journal of Abnormal Psychology, 107, 149±153. Kline, J. P., Blackhart, G. C., & Schwartz, G. E. R. (1999). Gender speci®city of resting anterior electroencephalographic asymmetry and defensiveness in the elderly. Journal of Gender-Speci®c Medicine, 2, 35±39. Kolb, B., & Whishaw, I. Q. (1996). Fundamentals of human neuropsychology (4th ed.). New York: W.H. Freeman and Company. Liotti, M., & Tucker, D. M. (1995). Emotion in asymmetric corticolimbic networks. In R. J. Davidson, & K. Hugdahl, Brain asymmetry (pp. 389±423). Cambridge: MIT. Mehrabian, A., & Russell, J. A. (1974). An approach to environmental psychology. Cambridge: MIT Press. Morris, J. D. (1995). Observations: SAM: The self-assessment manikin: an ecient cross-cultural measurement of emotional response. Journal of Advertising Research, 35, 63±68. Old®eld, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9, 97± 113. Russell, J. A., & Mehrabian, A. (1977). Evidence for a three-factor theory of emotions. Journal of Research in Personality, 11, 273±294. Schaer, C. E., Davidson, R. J., & Saron, C. (1983). Frontal and parietal electroencephalogram asymmetry in depressed and nondepressed subjects. Biological Psychiatry, 18, 753±762. Schraedley, P. K., Gotlib, I. H., & Hayward, C. (1999). Gender dierences in correlates of depressive symptoms in adolescents. Journal of Adolescent Health, 25, 98±108. Stanton, A. L., Dano-Burg, S., Cameron, C. L., & Ellis, A. P. (1994). Coping through emotional approach: Problems of conceptualization and confounding. Journal of Personality and Social Psychology, 66, 350±362. Sutton, S. K., & Davidson, R. J. (1997). Prefrontal brain asymmetry: A biological substrate of the behavioral approach and inhibition systems. Psychological Science, 8, 204±210. Tomarken, A. J., & Davidson, R. J. (1994). Frontal brain activation in repressors and nonrepressors. Journal of Abnormal Psychology, 103, 339±349. Tomarken, A. J., Davidson, R. J., & Henriques, J. B. (1990). Resting frontal brain asymmetry predicts aective responses to ®lms. Journal of Personality and Social Psychology, 59, 791±801. Tomarken, A. J., Davidson, R. J., Wheeler, R. E., & Doss, R. C. (1992). Individual dierences in anterior brain asymmetry and fundamental dimensions of emotion. Journal of Personality and Social Psychology, 62, 676±687. Wheeler, R. E., Davidson, R. J., & Tomarken, A. J. (1993). Frontal brain asymmetry and emotional reactivity: A biological substrate of aective style. Psychophysiology, 30, 82±89.
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Aective responses to EEG preparation and their link to resting anterior EEG asymmetry Ginette C. Blackhart *, John P. Kline, Keith F. Donohue, Steven D. LaRowe, Thomas E. Joiner Department of Psychology, Florida State University, Tallahassee, FL 32306, USA Received 18 September 2000; accepted 29 December 2000
Abstract Previous research relating anterior asymmetry in the electroencephalogram (EEG) to emotional states has not taken the aective context of the testing environment into account. This may be an important consideration, as the preparation procedures themselves are somewhat aversive. The purpose of this study was to assess whether self-reported mood state before and/or after EEG cap preparation was associated with EEG asymmetry. Mood state was assessed with the self-assessment manikin before and after the application of the electrode cap. Men and women showed a shift toward a more negative mood state postpreparation. Negative mood post-preparation, but not pre-preparation, predicted relative right frontal activation in men. In contrast, negative mood post-preparation, but not pre-preparation, predicted relative left frontal activation in women. Results are discussed as they relate to gender dierences in interpersonal engagement. # 2001 Elsevier Science Ltd. All rights reserved. Keywords: EEG; Gender dierences; EEG asymmetry
1. Introduction The experience of positive, approach-related behavior has been associated with left frontal and anterior temporal electroencephalographic (EEG) activation1, while the experience of negative, withdrawal-related behavior has been associated with right frontal and anterior temporal EEG activation (Ahern & Schwartz, 1985; Davidson, 1995; Heller, 1990; Tomarken, Davidson, & * Corresponding author. Tel.: +1-850-644-2040; fax: +1-850-644-7739. E-mail address: [email protected] (G.C. Blackhart). 1 Power in the alpha band is generally interpreted as an inverse index of brain activation (Davidson, 1995). For the rest of this paper, we will use ``activation'' to refer to a decrease in power in the alpha (e.g. 8±13 Hz) band. 0191-8869/01/$ - see front matter # 2001 Elsevier Science Ltd. All rights reserved. PII: S0191-8869(01)00015-0
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Henriques, 1990). Several lines of research converge to support this model. Victims of right and left frontal strokes show distinct aective changes (for a review, see Liotti & Tucker, 1995). Individuals with left frontal lesions due to stroke show more depressive and withdrawal behaviors, while people with right frontal lesions show more approach behavior, which can result in jovial mood, manic behavior, or pseudopsychopathy (Davidson, 1995; Kolb & Whishaw, 1996). Substantial research has documented the trait properties of the frontal EEG asymmetry (see Davidson, 1995, for a review), and a prediction from this literature is that left frontal active individuals should be more responsive to positive stimuli, whereas right frontal active individuals should be more responsive to negative stimuli. Davidson and Fox (1989) recorded baseline EEG measures from 10-month-old infants. Infants who were right frontally active during baseline later cried when separated from their mothers, while infants who were left frontally active did not cry in response to maternal separation. Tomarken et al. (1990) reported similar results in a study of adult women in response to emotionally salient ®lm clips. Women who showed increased right frontal activation at baseline were more likely to report a negative aective response to the aversive ®lm clips and a more globally negative mood. These results suggest that an individual's resting relative right frontal activation is linked to a lowered threshold for negative aective reactions to aversive stimuli (Tomarken et al., 1990). Similarly, relative left-frontal activation has been hypothesized to relate to a more global predisposition to experience positive mood. Consistent with this hypothesis, Tomarken, Davidson, Wheeler and Doss (1992) reported that women who demonstrated relative left anterior EEG activation reported increased positive aect and decreased negative aect compared with women who showed relative right anterior EEG activation. Jacobs and Snyder (1996) have reported a similar phenomenon in men. Furthermore, depressed individuals tend to exhibit decreased left frontal activation or increased right frontal activation (Gotlib, Ranganath, & Rosenfeld, 1998; Henriques & Davidson, 1990, 1991; Schaer, Davidson, & Saron, 1983). This phenomenon occurs during acute episodes of depression, but has also been observed in previously depressed individuals who are in remission (Allen, Iacono, Depue, & Arbisi, 1993; Henriques & Davidson, 1990), which again suggests that relative activation is related to a state-independent dispositional mood diathesis. Similarly, increased left frontal activation has been related to putative indicators of decreased vulnerability for depression (Harmon-Jones & Allen, 1997; Kline, Allen, & Schwartz, 1998; Kline, Blackhart, & Schwartz, 1999; Sutton & Davidson, 1997; Tomarken & Davidson, 1994). While EEG asymmetry has trait components, other research has demonstrated that frontal asymmetry responds to aective manipulations. For example, Ahern and Schwartz (1985) measured EEG in women who had just completed a task that was designed to elicit positive and negative aect. They reported that positive aect correlated with left frontal EEG activation, while negative aect correlated with right frontal activation. Similarly, Wheeler, Davidson, and Tomarken (1993) elicited positive and negative aect with emotional ®lm clips and found similar results in relative EEG activation. Related research suggests the association of left frontal activation with approach motivation, and the association of right frontal activation with withdrawal motivation (Davidson, 1992; Harmon-Jones & Allen, 1997; Sutton & Davidson, 1997). Though subjective mood at the time of testing has typically not correlated with frontal asymmetry (Tomarken & Davidson, 1994; Tomarken et al., 1990), the aect manipulations in these studies have used post-EEG preparation measures as their mood baseline (e.g. Tomarken et al., 1990). This assessment of baseline mood comes after the EEG preparation procedures, which
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may be somewhat unpleasant. The procedures include the ®tting of a tight cap to participants' heads, the abrasion of their scalps with a blunt probe, and the application of cold, wet electrode gel in the hair. The procedure usually requires 30 min to complete. Not surprisingly, participants appear to vary in their responses to this. Informal observations have some participants stoically enduring the procedure without a complaint, while some wince noticeably. Furthermore, other participants ask questions about the procedures, appear to be amused, and engage in conversations with the experimenters. The purpose of this study was to determine whether subjective mood correlates with frontal asymmetry after taking the EEG preparation into account. We were interested in whether: (1) the application of the EEG cap would produce a relative decrease in positive aect; and (2) whether the time of baseline mood assessment (i.e. pre or post-preparation) made a dierence in whether or not baseline mood predicted frontal asymmetry. As an additional exploratory measure, we assessed gender dierences in the relation between baseline mood and resting anterior asymmetry. 2. Method 2.1. Participants Thirty-six men and 41 women (all right handed) ranging in age from 16 to 39 (mean age=20.5, S.D.=3.70) volunteered to participate in the study. Participants were undergraduates in an Introduction to Psychology class, and received course credit for their participation. All men and women in the study interacted with an equal number of female and male experimenters. 2.2. Questionnaire administration and scoring Participants signed a consent form and completed questionnaires prior to EEG recording. Handedness was assessed with the Edinburgh Handedness Inventory (Old®eld, 1971). The selfassessment manikin (SAM) was used to measure pleasant mood (on the valence dimension) both before and immediately after participants were connected to the EEG cap. The SAM is a nonverbal method for quickly assessing valence, arousal, and dominance associated with an individual's emotional reaction to an event. It is an adaptation of the verbal semantic dierential scale developed by Mehrabian and Russell (1974), that measures emotions on three dimensions: pleasure-displeasure, arousal-nonarousal, and dominance-submissiveness. Mehrabian and Russell's semantic dierential scales showed sucient reliability, with 0.94 for pleasure-displeasure (Russell & Mehrabian, 1977). SAM ratings are highly related to the Mehrabian and Russell's semantic dierential scale, with a correlation of 0.97 for the pleasure-displeasure dimension (Bradley & Lang, 1994). Each scale ranges from 1 to 9, and on the pleasure-displeasure scale 1 indicates an unpleasant mood, 9 indicates a very pleasant mood, and 5 indicates a neutral mood. This scale corresponds to pictures of the SAM ®gure that range from smiling and happy to frowning and unhappy (Morris, 1995). Assessments with the SAM may elicit more consistent judgments concerning emotional reactions because the SAM ®gures are human-like (Bradley & Lang, 1994). For these reasons, the SAM pleasure-displeasure scale was judged to be a good measure of subjective pleasant mood both before and after EEG preparations.
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2.3. EEG recording and quanti®cation Resting EEG was recorded with a stretch lycra electrode cap with tin electrodes (Electrocap International, Eaton, Ohio) from a standard International 10-20 system of 19 channels referenced to linked ears. Data collection and reduction were accomplished with Neurolex software and a Neurosearch 24 data acquisition unit. Electrode gel was applied to each electrode, and the scalp at each site was gently abraded until impedances were below 10 k . Homologous leads (EEG and auricular leads) were within 1 k of each other. EEG records were visually examined for artifact, and epochs containing bioelectric artifact greater than 75 microvolts in any channel were rejected. Data were digitized on-line at 256 Hz (60 Hz notch ®lter enabled) during six 60 s periods, three with eyes open and three with eyes closed. Highpass ®lters were set at 2 Hz, and had a rollo of 6 dB per octave (®rst order), and lowpass ®lters were set at 64 Hz and had a rollo of 48 dB per octave (eighth order). Non-overlapping, artifact-free epochs of 256 samples (i.e. 1-s epochs) were extracted through a Hanning window and submitted to Fast Fourier Transform. Power was extracted in 1 Hz bins, which were combined into spectral bands. Average alpha (8±13 Hz) power (microvolts squared) was natural log transformed for normalization. A natural log transformation technique was used to normalize the distributions of power values, as these distributions tend to be positively skewed. This is consistent with the recommendations of Davidson, Ekman, Saron, Senulis, and Freisen (1990). Because alpha power has been found to be inversely related to the activation of the corresponding region of the brain, researchers have contended that anterior alpha asymmetry measurements re¯ect relative dierences in activity between the left and right hemispheres (Davidson, 1995). The alpha activity in the left side is subtracted from the alpha activity in the right side, and higher values indicate greater left-sided activation. Asymmetry scores were computed (log[right]-log[left]) for Fp2-Fp1, F4-F3, F8-F7, T4-T3, T6-T5, C4-C3, P4P3, and O2-O1. 2.4. Design and analysis In order to assess whether the preparation procedure was associated with a decrease in positive mood from pre to post-preparation, ANOVA was conducted for the pleasure dimension on the SAM from pre to post EEG cap preparation. General linear model analyses were conducted in order to assess whether T1 and/or T2 mood valence predicted ASYM for men and women. Time 1 mood (pre-preparation; T1), time 2 mood (post-preparation; T2), sex, T1SEX, and T2SEX were entered into the analysis. Follow-up analyses were conducted separately for women and men. 3. Results ANOVA revealed there was a signi®cant main eect for time F(1, 76)=13.49, P<0.001, where participants rated themselves as feeling signi®cantly less pleasant from T1 (M=5.91, S.D.=1.39) to T2 (M=5.40, S.D.=1.44). Zero order correlations show that for the entire sample, a signi®cant correlation was found between T1 and T2 mood. For men, a signi®cant correlation was found between T1 and T2
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mood. For women, signi®cant correlations were found between ASYM at F4-F3 and T2 mood, between ASYM at F8-F7 and T2 mood, and between T1 and T2 mood (Table 1). 3.1. Regression analyses There was a signi®cant multivariate interaction between T2 mood valence and sex F(8, 64)=2.72, P<0.02. The interaction of T1 mood valence and sex did not signi®cantly predict asymmetry F(8, 64)=1.06, P<0.40. There were signi®cant univariate eects at F4±F3 t(71)= 3.47, P<0.001 and at F8±F7 t(71)= 3.57, P<0.001, where the interaction of T2 mood valence and sex signi®cantly predicted asymmetry. No other signi®cant univariate eects were found at Fp2±Fp1, C4±C3, P4±P3, T4±T3, T6±T5, or O2±O1. In the follow-up analyses for men, T1 and T2 valence accounted for 11% of the variance in mid-frontal asymmetry (F4±F3) scores F(2, 33)=2.13, P<0.14, and 12% of the variance in lateral frontal asymmetry (F8±F7) scores F(2, 33)=2.31, P<0.12. The partial correlation of T2 mood with T1 mood partialed out signi®cantly predicted ASYM at F4±F3 =0.45, t(33)=2.06, P<0.05 and at F8±F7 =0.45, t(33)=2.06, P<0.05. Mood at T1 did not signi®cantly predict ASYM at F4±F3 (P<0.23) or at F8±F7 (P<0.38). T2 negative mood valence was associated with relative right frontal activation in men. In the follow-up analyses for women, T1 and T2 valence accounted for 25% of the variance in mid-frontal asymmetry, F(2, 38)=6.42, P<0.005, and 24% of the variance in lateral frontal asymmetry, F(2,38)=5.92, P<0.01. The partial correlation of T2 mood with T1 mood partialed out signi®cantly predicted ASYM at F4±F3 = 0.51, t(38)= 2.93, P<0.01 and at F8±F7 = 0.56, t(38)=±3.19, P<0.01. Mood at T1 did not predict ASYM at F4±F3 (P<0.88) or at F8±F7 (P<0.42). T2 negative mood valence was associated with relative left frontal activation in women.
Table 1 Zero order correlations between assymmetry (ASYM), Time 1 (T1) mood, and Time 2 (T2) mood ASYM Entire sample ASYM T1 Valence T2 Valence Men ASYM T1 Valence T2 Valence Women ASYM T1 Valence T2 Valence *P< 0.05
T1 valence
T2 valence
±
0.11 ±
0.08 0.64* ±
±
0.02 ±
0.27 0.66* ±
±
0.29 ±
0.50* 0.59* ±
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4. Discussion Overall, the EEG cap application appeared to lead to a less positive mood. Given the nature and duration of the procedure, this is hardly surprising. Since psychophysiological measurements are often used for subtle assessments of emotional functioning, this result underscores the importance of taking the measurement context into account when interpreting EEG asymmetry/ mood relations. The measures of mood most proximate to the EEG recordings were associated with asymmetry when the results of pre-cap preparation mood ratings were statistically controlled. Pre-cap preparation mood measures were unrelated to EEG asymmetry. This suggests that the mood/EEG relations that we described in this study were very much state-speci®c. The gender dierence obtained in this study was unexpected, and is dicult to interpret. While male participants met predictions by showing a positive association, albeit a weak one, between pleasantness and asymmetry, the result was opposite and more robust for women. Not only were these results for female participants contrary to the predictions of the study, but were also inconsistent with other research that assessed female participants' reactions to negative stimuli (Davidson & Fox, 1989; Tomarken et al. 1990). In this context, the nature of our study's negative stimulus Ð the preparation procedure Ð is important to consider. The procedure, although certainly mildly aversive, also includes a buering interpersonal in¯uence; namely, the experimenter, whose presence and supportive words may be reassuring to participants, especially to particular participants (e.g. women). Importantly, negative stimuli used in other studies, such as an aversive ®lm clip, probably do not contain this buering in¯uence. We suggest that this interpersonal buer had two eects on women, more so than on men: (1) women were more interpersonally engaged with the experimenter than were men (and engagement has been shown to contribute to relative left frontal activation); and (2) in part because women were more interpersonally engaged and thus felt more supported, they were more emotionally expressive than men about the context (and here, the context of the preparation was mildly aversive, perhaps encouraging expression of negative emotion among women). Women who became more engaged with the entire context, including with the experimenter, may have been more likely to display left frontal activation and more likely to vent emotions about the context, producing the association between left frontal activation and negative mood in women. By contrast, men may have been less aected by or less responsive to the buering eects of the experimenter, and thus may have experienced the preparation procedure as uniformly negative, much as if they had been viewing an aversive ®lm clip; and, in our regression analyses, ®ndings from men mirrored ®ndings from studies using aversive ®lm clips and other similar stimuli Ð right frontal activation was associated with negative mood among men. We emphasize that this is a speculative explanation, in need of empirical scrutiny. However, past research lends some credence to elements of this explanation. For example, there is some indication that women are more ``engageable'' than men, in that they endorse more aliative needs than men (e.g. Cheng, 1999), and appear to be more protected by social support and to value it more highly than men (e.g. Barker, Morrow, & Mitteness, 1998; Schraedley, Gotlib, & Hayward, 1999). Moreover, there is some indication that women, more so than men, may constructively cope with adversity by expressing negative emotions (Stanton, Dano-Burg, Cameron, & Ellis, 1994).
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In sum, we predicted that left frontally active participants in this study would ®nd the process of EEG cap application less aversive than those who were right frontally active. This result was obtained for men, but women showed the opposite result. Future research may wish to pay attention to contextual and preference factors that might mediate such gender dierences in anterior asymmetry/mood relationships, and may also wish to focus on gender dierences in interpersonal engagement as it relates to anterior asymmetry. Future EEG research also needs to pay careful attention to the fact that psychophysiological research, strictly speaking, never truly measures traits per se, but only those traits as they interact with our experimental protocols. This leaves the possibility of trait/state interactions in all of our data, even when experiments are designed to speci®cally measure traits. We assume that by holding our procedures constant across participants, all participants will respond similarly to the procedures that we do not typically think of as manipulations (e.g. EEG preparation, interaction with the experimenter, etc.). Therefore, we need to develop some way to better measure basal trait EEG. One possibility is to introduce a relaxation phase to the participants after the EEG cap preparation in an attempt to observe stabilized trait anterior asymmetry. This way a basal ratio can be obtained dynamically prior to a speci®c experimental manipulation. Another possibility is to use a less invasive procedure, such as a geodesic sensor net (Electrical Geodesics Incorporated, Eugene, OR). This system allows for the placement of electrolyte-impregnated sponges on the participant's scalp, and does not necessitate extensive scalp abrasion. These two methods may allow for less procedural reactivity, allowing for a better estimate of basal, trait asymmetry. References Ahern, G. L., & Schwartz, G. E. (1985). Dierential lateralization for positive and negative emotion in the human brain: EEG spectral analysis. Neuropsychologia, 23, 745±756. Allen, J. J., Iacono, W. G., Depue, R. A., & Arbisi, P. (1993). Regional electroencephalographic asymmetries in bipolar seasonal aective disorder before and after exposure to bright light. Biological Psychiatry, 33, 642±646. Barker, J. C., Morrow, J., & Mitteness, L. S. (1998). Gender, informal social support networks, and elderly urban African Americans. Journal of Aging Studies, 12, 199±222. Bradley, M. M., & Lang, P. J. (1994). Measuring emotion: the self-assessment manikin and the semantic dierential. Journal of Behavioral Therapy and Experimental Psychiatry, 25, 49±59. Cheng, C. (1999). Gender-role dierences in susceptibility to the in¯uence of support availability on depression. Journal of Personality, 67, 439±467. Davidson, R. J. (1995). Cerebral asymmetry, emotion, and aective style. In R. J. Davidson, & K. Hugdahl, Brain asymmetry (pp. 361±387). Cambridge: MIT. Davidson, R. J. (1992). Anterior cerebral asymmetry and the nature of emotion. Brain and Cognition, 20, 125±151. Davidson, R. J., Ekman, P., Saron, C., Senulis, J., & Freisen, W. V. (1990). Approach/withdrawal and cerebral asymmetry: emotional expression and brain physiology, I. Journal of Personality and Social Psychology, 58, 330±341. Davidson, R. J., & Fox, N. A. (1989). Frontal brain asymmetry predicts infants' response to maternal separation. Journal of Abnormal Psychology, 98, 127±131. Gotlib, I. H., Ranganath, C., & Rosenfeld, J. P. (1998). Frontal EEG alpha asymmetry, depression, and cognitive functioning. Cognition and Emotion, 12, 449±478. Harmon-Jones, E., & Allen, J. J. B. (1997). Behavioral activation sensitivity and resting frontal EEG asymmetry: covariation of putative indicators related to risk for mood disorders. Journal of Abnormal Psychology, 106, 159±163. Heller, W. (1990). The neuropsychology of emotion: Developmental patterns and implications for psychopathology. In N. Stein, B. L. Leventhal, & T. Trabasso, Psychological and biological approaches to emotion (pp. 167±211). Hills ale, NJ: Erlbaum.
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