Cerebral Cortex Advance Access originally published online on January 11, 2007
Cerebral Cortex 2007 17(11):2526-2535; doi:10.1093/cercor/bhl158
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Cognitive Coping Style Modulates Neural Responses to Emotional Faces in Healthy Humans: A 3-T fMRI Study
1 Department of Psychiatry, University of Münster, Germany, 2 Department of Clinical Radiology, University of Münster, Germany, 3 IZKF Group 4, Department of Psychiatry and IZKF Münster, University of Münster, Germany
Address correspondence to Thomas Suslow, Department of Psychiatry, School of Medicine, University of Münster, Albert-Schweitzer-Str. 11, 48149 Münster, Germany. Email: Thomas.Suslow{at}ukmuenster.de.
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Abstract |
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Repression designates coping strategies that aim to shield the organism from distressing stimuli by disregarding their aversive characteristics. In contrast, sensitization comprises coping strategies that are employed to reduce situational uncertainty such as analyzing the environment. Functional magnetic resonance imaging was used to study neural correlates of coping styles during the perception of threatening and nonthreatening socially relevant information. Pictures of human faces bearing fearful (ambiguously threatening), angry (unambiguously threatening), happy (nonthreatening), and neutral expressions were presented masked and unmasked. Two groups of subjects were examined who were defined as consistent repressors versus consistent sensitizers with the Mainz Coping Inventory. Sensitizers tended to exhibit stronger neural responses in the amygdala to unmasked fearful faces compared with repressors. Overall, repressors were cortically more responsive to fearful (ambiguously threatening) and happy (nonthreatening) facial expressions than sensitizers, whereas sensitizers presented an enhanced responsivity to angry faces in several prefrontal areas, that is, unambiguously threatening expressions. Results from time series analyses suggest that sensitizers could exhibit less top-down cortical regulation of the amygdala than repressors in the processing of fearful faces. An increased responsivity of the amygdala to ambiguously threatening stimuli may represent a biological determinant of sensitizers' feelings of uncertainty.
Key Words: facial expression • fear • repression • sensitization • threat processing
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Introduction |
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The term "repression" was introduced by Freud in the late 19th century (Freud 1926/1940–1942
). He defined it as turning something away and keeping it at a distance from the conscious. In the late 1970s, Weinberger et al. (1979) used measures of anxiety and defensiveness to identify repressive coping on an empirical basis. Since then a large number of studies have been defining cognitive and physiological correlates of coping styles (Furnham et al. 2003). Considerable evidence has emerged that possessing a repressive coping style is associated with adverse physical health (Myers and Derakshan 2004).
In most coping approaches avoidance and vigilance have been conceptualized as ends of a unidimensional continuum (repression sensitization, Byrne 1961), or no specification with regard to the interrelationship of these variables was made (blunting-monitoring, Miller 1987). In the model of coping modes proposed by Krohne (1989, 1993) these tendencies are conceived as independent or separate personality dimensions. The term coping mode refers to the specific configuration of an individual's standing on both dimensions. The habitual employment of vigilant strategies or avoidant ones does not preclude each other. However, research based on the model of coping modes has primarily focused on those individuals who score high for one tendency but low for the other. High habitual avoidance together with low habitual vigilance should be reflected in consistent avoidance. Individuals with such a behavior pattern are labeled consistent avoiders or according to the traditional coping research "repressors," whereas persons manifesting high habitual vigilance and low cognitive avoidance are called consistent vigilants or "sensitizers" (Krohne 1989, 1993). Krohne and colleagues constructed the Mainz Coping Inventory (MCI) to assess dispositional preferences for vigilant and avoidant coping strategies in threatening situations (Krohne and Egloff 1999; Krohne et al. 2000).
The model of coping modes extends beyond earlier approaches in coping research by relating the descriptive terms of vigilance and avoidance to an explicative basis. This model assumes that emotional arousal stimulates the tendency to cognitively avoid threat-related information, whereas uncertainty activates vigilant behavioral tendencies (Krohne 1993). Consistent avoiders or repressors have the cognitive coping strategy to minimize the emotional impact of threatening stimuli. Repressors withdraw their attention from and curtail the processing of threatening aspects of situations. Threat-related information is faded-out during information gathering in repressors. Repressors have repeatedly shown to exhibit higher physiological arousal (e.g., enhanced cardiovascular responses) than sensitizers when confronted with threatening stimuli (Cook 1985; Kohlmann et al. 1996; Rohrmann et al. 2002). The intense physiological reactions of repressors are supposed to be associated with an increased risk of health problems (Pennebaker and Traue 1993). Sensitizers' inability to tolerate uncertainty promotes an extensive monitoring and analyzing of the environment with respect to the appearance of danger signals.
So far very few studies exist in which brain activation has been examined as a function of coping style. Findings from resting electroencephalographic research suggest that frontal brain areas may play an important role in repressive coping (Tomarken and Davidson 1994; Kline et al. 1998). To our knowledge, up to now there is only one functional magnetic resonance imaging (fMRI) study examining cerebral activation in repression (Sander et al. 2003). Identification tasks with acoustically presented sad and happy intonations were administered to healthy repressive women. Interestingly, independent of the task orbitofrontal cortical activation was larger for repressors than for nonrepressors. During the identification of sad intonations repressors showed larger left than right hemisphere activation in temporo-parietal regions, which include the auditory cortex and sensory speech areas. Nonrepressors manifested a larger right than left hemisphere activation instead. However, different coping styles were not characterized by a general difference of cortical lateralization.
Facial expression serves as an important social signal of imminent environmental conditions. Discrete emotion theorists claim that people express a limited number of (blends of) basic emotions (Ekman 1984; Izard 1991). Of the many visual cues that can indicate social threat, facial emotions have most widely been investigated with neuroimaging techniques. The facial expression of fear signals potential danger in the environment but gives little information about the source or location of that threat. Angry faces are also signals of potential danger but they indicate the source of the threat.
Using fMRI and other approaches, researchers have identified a structural network encompassing the orbitofrontal cortex, amygdala, anterior cingulate cortex, and occipitotemporal visual cortical regions that consistently participates in the processing of emotional faces (Morris et al. 1998; Davis and Whalen 2001; Kesler-West et al. 2001; Adolphs 2002; Phillips et al. 2003). This network appears to be also involved when faces are presented below the level of conscious awareness (Whalen et al. 1998; Etkin et al. 2004; Killgore and Yurgelun-Todd 2004; Nomura et al. 2004; Liddell et al. 2005). Besides the amygdala, occipitotemporal face processing areas appear to be consistently activated during the nonconscious processing of facial emotion (Killgore and Yurgelun-Todd 2004; Phillips et al. 2004; Liddell et al. 2005). There is evidence that the amygdala has a central role in the processing of fearful facial expression (Morris et al. 1996; Williams et al. 2004) but is also involved in the processing of angry, sad, and happy expressions (Breiter et al. 1996; Wright et al. 2002; Yang et al. 2002). Other prefrontal areas such as the ventral and dorsal prefrontal cortices (PFCs) also interact with the amygdala via projections to the orbital PFC as well as via thalamic and striatal circuits (Hariri et al. 2000, 2003). The cognitive regulation of emotion such as the inhibition of negative emotion and in particular the cognitive control of attention to threat-related stimuli is considered to be implemented by a network of cortical areas including orbitofrontal (Brodmann's area [BA] 11), ventrolateral (BAs 46, 47) and dorsolateral (BA 9) PFC and the anterior cingulate (BAs 24, 25, 32) (Beauregard et al. 2001; Cardinal et al. 2002; Ochsner et al. 2002, 2004; Phan et al. 2002, 2005; Bishop et al. 2004). Prefrontal cortical areas (BAs 10, 11, 47) and the anterior cingulate were found to be functionally connected with the amygdala (Hariri et al. 2003; Das et al. 2005; Pezawas et al. 2005): The PFC has a modulatory role on amygdala responses—even when responses in the amygdala are evoked by masked emotional signals (Nomura et al. 2004). Cognitive inhibition of negative emotion increases activity in the PFC and attenuates limbic responses.
The present study used 3-T fMRI to investigate differences in brain reactivity to biologically anchored threat-relevant social signals (i.e., ambiguously threatening (fearful), unambiguously threatening (angry), and nonthreatening (happy) emotional expression) as a function of coping style. The MCI was used to assess coping style (Krohne and Egloff 1999; Krohne et al. 2000). We decided to apply a passive viewing task because previous findings indicate a more robust activation of the amygdala (and the visual processing system) in response to facial emotions under simple viewing or implicit processing conditions than during performance of explicit emotion processing tasks (Critchley, Daly, et al. 2000; Lange et al. 2003). Krohne and colleagues hypothesized that repressors differ from sensitizers on a preattentive and a controlled information processing level by inhibiting the processing of threat-related information (Krohne 1978, 1993; Hock and Egloff 1998; Krohne et al. 2000). We expected that a sensitizing style is associated with greater activation of the amygdala in response to a threatening facial expression, which may be particularly accentuated to ambiguously threatening (i.e., fearful) faces because sensitizers have difficulties tolerating uncertainty. In addition, we hypothesized larger differences between repressors and sensitizers regarding amygdala activity in case of high visibility of facial emotion because repressors' anterior cingulate/prefrontal network, which is responsible for cognitive control of emotions, should be more engaged in the inhibition of the amygdala when threats are clearly visible. Thus, it was also hypothesized that repression is associated with an increased activation of the anterior cingulate/prefrontal network in response to threatening emotions compared with sensitization, especially in case of high visibility of facial emotions. Based on theoretical considerations it can be assumed that when confronted with fearful faces sensitizing individuals produce strong activations in brain systems that are responsible for engagement and control of visual attention (a fronto-parietal network including the visual system and the pulvinar; e.g., Kastner and Pinsk 2004). The present study may help to clarify the question whether activation of the visual processing system in response to threatening information is more pronounced in sensitizers than in repressors.
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Materials and Methods |
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Participants
Twenty healthy, right-handed university students (10 females and 10 males) participated in this fMRI study. Handedness was defined by the Handedness Questionnaire (Raczkowski et al. 1974). All subjects had no history of psychiatric or neurological illness were free of psychotropic medication and had normal or (by contact lenses) corrected-to-normal vision. The DIA-X interview (Diagnostisches Expertensystem für Psychische Störungen, Wittchen and Pfister 1997), a standardized psychiatric screening interview, was administered to assess current and past psychiatric symptomatology. Study participants were selected from a sample of 150 students on the basis of their scores on the MCI (Krohne et al. 2000). Ten persons with high scores on the cognitive avoidance scale (>75th percentile of the screening sample) and low scores on the vigilance scale (<25th percentile) were included as consistent repressors in the present study, whereas 10 persons with high scores on the vigilance scale (>75th percentile of the screening sample) and low scores on the cognitive avoidance scale (<25th percentile) were included as consistent sensitizers. Repressors differed significantly (Ps < 0.001) from sensitizers on both MCI scales (see Table 1). Subjects were screened for imaging safety concerns, and gave their informed, written consent to the study, which was approved by the institutional ethics committee. All subjects received a compensation of 20 EUR after their participation in the fMRI experiment.
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Repressors and sensitizers were matched for sex and did not differ in their mean age and verbal intelligence (as measured by the German adaptation of the Wechsler Adult Intelligence Scale revised version; WAIS-R, Tewes 1991
) (Ps > 0.30). The Differential Emotions Scale (DES) (Izard et al. 1974) was administered after the fMRI experiment to assess state emotions during image presentation. Sensitizers and repressors did not differ in their emotions felt during the fMRI experiment in the scanner (Ps > 0.14). The State-Trait-Anxiety Inventory (STAI; Spielberger et al. 1970; Laux et al. 1981) was administered to measure trait anxiety. As could be expected, sensitizers had higher STAI trait anxiety scores than repressors (t(18) = 4.30, P < 0.01). Stimulus Materials and Procedure
The MCI is a stimulus-response inventory (Krohne et al. 2000) that assesses habitual preferences for vigilant and cognitive avoidant coping strategies in 4 ego-threatening (e.g., public speaking) and 4 physically threatening situations (e.g., driving with an inexperienced driver). For each situation, 5 vigilant or sensitizing items (e.g., information search, anticipation of negative events) and 5 cognitively avoidant or repressive items (e.g., denial, attention diversion) are administered in a true–false response format. To yield scores of habitual coping preferences, scored answers are summed for vigilant and avoidant items across all 8 situations. Employing a latent-class analysis Schmukle et al. (2000) were recently able to identify the presumed coping patterns of repression and sensitization for the MCI in a large sample of healthy probands. The STAI (Spielberger et al. 1970), a measure of anxious emotional and cognitive reactions, was administered in its trait form (German adaptation of Laux et al. 1981). The DES (Izard et al. 1974; Kotsch et al. 1982) in its state form assesses the intensity of fundamental emotions. The DES consists of 30 adjectives (items) and 10 emotion scales: 7 negative emotions (sadness, anger, disgust, contempt, fear, shame, and guilt) and surprise, interest, and joy. The intensity of emotion experience is assessed on a 4-point scale (0–3). The DES was used in its German adaptation of Merten and Krause (1993).
Facial stimuli consisted of gray-scale normalized fearful (F), angry (A), happy (H), and neutral (N) expressions of 10 individuals (Ekman and Friesen 1976). Thus, 40 pictures were presented in the fMRI experiment. Subjects saw alternating epochs of emotional faces or a no-face control stimulus (a gray rectangle). Facial stimuli were randomly presented. Each trial had a duration of 500 ms. Within masked epochs, which always preceded the unmasked epochs, emotional faces were shown for 33 ms, that is, probably below the threshold of conscious awareness (Esteves and Öhman 1993), followed immediately by a 467-ms neutral expression. In unmasked epochs facial expression was shown for 500 ms. The no-face control stimulus was shown for 450 ms followed by a blank screen for 50 ms. The experiment was realized by means of the software package Experimental Run Time System (Beringer 1999). An intelligent preload algorithm is built into the runtime system managing the image switching process and allowing to realize each onset within one video refresh.
The order of epochs was counterbalanced across subjects. There were 4 counterbalanced orders of presentation (Latin square design) [1. c (no-face control epoch), A, c, F, c, H, c, N, c, A, c, F, c, H, c, N; 2. c, F, c, N, c, A, c, H, c, F, c, N, c, A, c, H; 3. c, N, c, H, c, F, c, A, c, N, c, H, c, F, c, A; 4. c, H, c, A, c, N, c, F, c, H, c, A, c, N, c, F]. Thus, each face epoch was preceded by a no-face control epoch and was presented twice, so that the overall presentation time for the masked and the unmasked experiment was 8 min, respectively.
In a preliminary experiment, the face stimuli of Ekman and Friesen (1976) had been presented to an independent sample (10 females and 10 males; age M: 28.4 years; standard deviation [SD]: 8.4 years) in our laboratory with the task to identify the emotional quality of the masked faces. In this experiment, masked faces were presented for 33 ms, followed immediately by a 333-ms neutral expression. A force choice paradigm with 4 response categories was used (neutral and 3 emotions). The mean sensitivity index d' of study participants was 0.49. That is, study participants performed at chance level (0.5) and were not able to consciously discriminate between facial expressions.
Subjects were instructed that they would see human faces and that they should pay attention to them. Images were presented via projection to the rear end of the scanner (Sharp XG-PC10XE with additional high frequency shielding). The head position was stabilized with a vacuum head cushion.
fMRI Data Acquisition and Data Analysis
T2* functional data were acquired at a 3-Tesla scanner (Gyroscan Intera 3T, Philips Medical Systems, Best, The Netherlands) using a single shot echoplanar sequence with parameters selected to minimize distortion while retaining adequate signal to noise ratio and T2* sensitivity, according to suggestions made by Robinson et al. (2004). Volumes consisting of 25 axial slices were acquired (matrix 1282, resolution 1.75 mm x 1.75 mm x 3.5 mm; time repetition = 3 s, time echo = 30 ms, flip angle = 90°) 160 times in block design, 10 times per condition. To optimize the following normalization procedures, the same sequence parameters were used to cover the whole brain with 43 slices. T1-weighted inversion recovery and a high-resolution T1-weighted 3D sequence (isotropic pixel, 0.5 mm3) were also acquired. Functional imaging data were motion corrected, using a set of 6 rigid body transformations determined for each image, spatially normalized to standard MNI space (Montreal Neurological Institute) and smoothed (Gaussian kernel, 6-mm full-width at half-maximum) using Statistical Parametric Mapping 2(Wellcome Department of Imaging Neuroscience, London, UK). Checks on motion artifacts were performed by rerunning the analyses using the estimated motion parameters as covariates of no interest in the design matrix and confirming that the results were unaffected. Statistical analysis was performed by modeling the different conditions (angry, fearful, happy, and neutral) as variables within the context of the general linear model (convolved with a standard hemodynamic response function).
The amygdala (Tzourio-Mazoyer et al. 2002) and 4 prefrontal areas (BAs 10, 11, 25, and 47; Lancaster et al. 2000) were selected as regions of interest (ROIs). Voxel values of the ROIs were extracted, summarized by mean, and tested among the different conditions using the MarsBaR toolbox (Brett et al. 2002). To investigate brain activity in the processing of facial emotion, fMRI data obtained in response to masked and unmasked emotion faces were subtracted from those obtained in response to neutral faces. Activation data (contrast values) were analyzed by means of 2 x 3 x 2 analyses of variance with one between-group independent variable (coping style [repression vs. sensitization]) and 2 repeated-measures independent variables (emotion face condition [fear, anger, and joy], and laterality [left vs. right]) for each visibility condition (masked vs. unmasked) separately. Post hoc analyses (Tukey honest significant difference tests) were focused on the effects involving coping style. ROI analyses were made with significance levels set at P < 0.05 (uncorrected). In addition, a voxel-wise ROI analysis was conducted for the amygdalae. Bilateral amygdala responses to emotion faces compared with neutral faces were investigated. This analysis was conducted at P < 0.05, corrected for multiple comparisons across the amygdalae.
A whole-brain analysis was conducted to determine brain regions, which are differentially activated as a function of repressive and sensitizing coping style. For each visibility condition (masked vs. unmasked), activation data (t maps) were calculated for each subject in each of the 3 emotion face conditions (fearful, angry, and happy) relative to the neutral face control condition. Firstly, one-sample t-tests was performed on activation data for each emotion condition to determine main effects of emotions. Secondly, random effects analysis (t-tests for independent samples) was made to examine brain activation differences between groups. For a priori ROIs, the significance level in the whole brain analyses was put at P < 0.001 (uncorrected) with clusters defined by at least 3 contiguous voxels of significant response. This low cluster threshold (which was also applied in other recent fMRI studies; e.g., Thomas et al. 2001; Egner and Hirsch 2005) was chosen to maximize sensitivity in the detection of activation differences between study groups. Activations in other brain regions were evaluated at an False Discovery Rate-corrected threshold of P < 0.05. A priori ROIs in our whole brain analysis were several prefrontal areas (BAs 10, 11, 47), the anterior cingulate, and temporo-occipital cortical areas (inferior/middle occipital gyrus (BA 18), fusiform gyrus (BAs 19, 37), and superior temporal gyrus (BAs 13, 22, 41, 42)) known to be involved in emotion regulation and/or the processing of facial emotions (e.g., Morris et al. 1998; Davis and Whalen 2001; Kesler-West et al. 2001; Adolphs 2002; Ochsner et al. 2002, 2004; Phan et al. 2002, 2005; Phillips et al. 2003; Killgore and Yurgelun-Todd 2004; Ishai et al. 2005; Liddell et al. 2005).
Anatomical labels of reported coordinates (transformed from MNI to Talairach space) of peak clusters were retrieved from the Talairach Daemon database (Lancaster et al. 2000) within a 5-mm cubical search range. Functional connectivity is defined as the (undirected) correlation between 2 or more fMRI time series recorded from distributed brain regions. To evaluate the interdependency of brain regions involved in emotion regulation during the presentation of threatening information compared with that of neutral information correlations between MR signal time courses of the amygdala and 4 prefrontal ROIs (BAs 10, 11, 25, and 47) were specified for (masked and unmasked) fear, angry, and neutral face epochs separately. To evaluate the extent to which amygdala activation and amygdala-prefrontal regions (BAs 10, 11, 25, and 47) coupling are correlated with cognitive avoidance and vigilance (as measured by the MCI), correlations were calculated for each emotion condition. However, because almost no correlations of MCI coping dimensions with amygdala activation or coupling were found we will report in the following only the results from our categorical analyses.
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Results |
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ROI Analysis: Amygdala
Masked Face Presentation
Results from a 2 x 3 x 2 analysis of variance based on contrast values yielded no significant main or interaction effect for the masked face condition.
Unmasked Face Presentation
A significant main effect of emotion condition was observed for the amygdala in the unmasked face condition (F2,17 = 5.24, P < 0.05, partial eta squared = 0.38). According to post hoc tests amygdala activation to happy faces and to fearful faces was greater than that to anger faces (see Fig. 1). In addition, there was an interaction between coping style and emotion condition that just failed to reach statistical significance (F2,17 = 3.47, P = 0.054, partial eta squared = 0.29). No other significant effects were observed. The partial eta squared for the interaction indicates a rather small effect size. Sensitizing individuals had higher contrast values than repressive individuals in the fearful face condition (P < 0.05) but did not differ from repressive individuals for the anger face and the happy face condition (see Fig. 2). Thus, sensitizing persons tended to show more activation of the amygdala in response to fearful faces than repressive persons. A power analysis calculated with GPOWER (Erdfelder et al. 1996) indicates that our analysis of variance on amygdala contrast values had a power to detect a large (d = 0.40) interaction effect (such as that between group and emotion condition) of only 0.28. Taking the small sample size into account this low value is not surprising.
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The voxel-wise ROI analysis of the amygdalae yielded significant between-group differences in the (unmasked) fearful face condition. Sensitizing individuals showed stronger activation responses to fear faces in the left and right amygdala compared with repressive individuals (see Fig. 3).
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ROI Analysis: Prefrontal Areas
Masked Face Presentation
Results from 2 x 3 x 2 analyses of variance based on contrast values yielded no significant main or interaction effect in the masked face condition for any of our prefrontal ROIs (BAs 10, 11, 25, and 47).
Unmasked Face Presentation
According to results from further analyses of variance based on contrast values, there was also no significant main or interaction effect in the unmasked face condition for any of the prefrontal ROIs (BAs 10, 11, 25, and 47).
Whole-Brain Analysis
Masked Face Presentation: Effects of Emotion Condition
Whole-brain analysis revealed no significant responses to masked fear expression (see Table 2). Masked presentation of anger expression activated the right temporal lobe and middle occipital gyrus. Finally, masked presentations of happy faces activated the superior temporal gyrus in the right hemisphere. Thus, masked angry as well as masked happy faces caused activation in the (right) superior temporal gyrus.
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Masked Face Presentation: Between-Group Comparisons
Compared with repressors there were no brain regions in which sensitizers demonstrated increased activation to fearful (vs. neutral) facial expression (see Table 3). Compared with sensitizing individuals repressive individuals exhibited enhanced bilateral anterior cingulate activation and left temporal and occipital lobe activation in response to fearful faces.
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Results from our between-group analysis indicated an increased activation of the right middle frontal gyrus to masked angry faces in sensitizing individuals. Masked angry faces caused stronger activation of the right superior temporal gyrus in repressors compared with sensitizers.
Sensitizing individuals demonstrated a significantly greater neural response to facial expressions of happiness than repressive individuals in the left lingual gyrus (see Table 3). To happy faces, repressors exhibited greater neural response than sensitizers in the left fusiform gyrus and right middle occipital gyrus.
Unmasked Face Presentation: Effects of Emotion Condition
Unmasked presentation of emotion faces produced more activation differences compared with neutral faces than masked presentation of emotion faces (see Table 4). According to the results of our whole-brain analysis, fearful faces caused significant activation in the left superior frontal gyrus. Further brain structures activated in response to fearful facial expression included both fusiform gyri and several other face processing structures of the temporal and occipital lobes.
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There were significant responses to (unmasked) anger expression in parts of the left prefrontal lobe (BA 10) and visual processing regions of the occipital lobe bilaterally. Presentations of happy faces activated several face processing structures of the temporal and occipital lobes bilaterally.
Unmasked Face Presentation: Between-Group Comparisons
Compared with repressors there were no brain regions in which sensitizers demonstrated increased activation to fearful (vs. neutral) facial expression (see Table 5). Repressive individuals instead showed an enhanced activation of the right middle frontal gyrus (BA 10) and the right fusiform gyrus.
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For unmasked angry facial expression sensitizers showed, compared with repressors, enhanced frontal lobe activation. Instead, repressive individuals responded with stronger activation of (occipital) face processing structures to angry facial expression than sensitizing individuals.
There were no clusters of significantly increased activation in sensitizers compared with repressors for (unmasked) happy faces. For happy facial expression, repressors showed, compared with sensitizers, enhanced frontal lobe activation. Furthermore, repressors also exhibited a stronger activation of visual processing structures to happy facial expression in the temporal and occipital lobes than sensitizing individuals.
Functional Connectivity between Amygdala and Prefrontal Regions: Between-Group Comparisons
Results from our time series analyses indicate that temporal relationship between activation of the amygdala and activation of prefrontal areas (BAs 10, 11, 25, and 47) was similar for repressors and sensitizers during their neural response to masked fearful and masked angry faces (see Table 6). In the case of (masked) neutral facial expression, percentages of shared variance between activation course of the amygdala and that of orbitofrontal and medial prefrontal regions (BAs 11 and 25) were significantly higher in repressors than in sensitizers. However, in these conditions mean correlations between amygdala and prefrontal activation were rather low for both groups.
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Temporal relationship between activation of the amygdala and activation of prefrontal areas (BAs 10, 11, 25, and 47) was similar for repressors and sensitizers during their neural response to unmasked angry and neutral faces (see Table 7). In the case of unmasked fearful facial expression, percentage of shared variance between amygdala activation and activation of the ventromedial prefrontal region (BA 10) was higher in repressors (50.8%) than in sensitizers (29.1%). Thus, between repressors time courses of neural activation of the amygdala and the anterior-polar prefrontal region appear to be more closely associated than between sensitizers.
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Discussion |
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We studied the impact of cognitive coping styles on cerebral activation patterns during the processing of threatening and nonthreatening facial emotions. Specific and more general patterns of activation differences were observed between the repressors and sensitizers. According to the model of coping modes (Krohne 1989
, 1993) repressors have the cognitive coping strategy to minimize the emotional impact of threatening stimuli by withdrawing their attention from and curtailing the processing of threatening information. Sensitizers' inability to tolerate uncertainty should instead promote an extensive monitoring and analyzing of the environment. Sensitizers tended to show a stronger activation of the amygdala in response to clearly visible fearful faces than repressive persons. Even though the relevant interaction effect (just) failed to reach the conventional level of significance (P < 0.05) one should be cautious to reject a differential activation hypothesis because statistical power is low in the present study due to small sample size (consequently the risk of committing a type II error is rather high). In the masked fearful face condition no group difference in amygdala activation was found. Group differences were not significant for activation of the amygdala during the presentation of angry (i.e., unambiguous threatening) or happy (i.e., positive) faces, regardless of visibility. Thus, the increased response tendency in sensitizing individuals is selective for ambiguously threatening faces. The facial expression of fear indicates the presence of danger in the environment but, in contrast to angry faces, not its source. This increased responsivity of the amygdala to ambiguously threatening stimuli may represent a biological determinant of sensitizers' feelings of uncertainty and apprehension. Because sensitizers showed less activation of the (right) ventromedial PFC (BA 10) than repressors in response to unmasked fearful faces and activations of amygdala and ventromedial PFC were temporally less closely related during the processing of unmasked fearful faces in sensitizers than in repressors it appears that sensitizers could exhibit less top-down cortical regulation of the amygdala than repressors.
Repressors manifested a stronger activation of the fronto-cortical network of emotion control than sensitizers in response to fearful expression (i.e., the anterior cingulate [BA 24] in the masked presentation condition and the [right] ventromedial PFC [BA 10] in the unmasked presentation condition). Independent of presentation condition repressors were found to respond more strongly with activation of temporo-occipital visual systems to fearful faces than sensitizing individuals. Thus, there was no evidence that repressors withdraw their attention from or curtail the processing of threat indicating facial expression. The enhanced visual activation in repressors might be associated with increased attention to the ambiguous threatening expressions. We found no support for the hypothesis that sensitizers produce stronger activations in brain systems that are responsible for the engagement of visual attention, a fronto-parietal network including the visual system.
Unlike for fearful faces, in case of angry faces sensitizers showed stronger activation of frontal cortical areas than repressors (the ventromedial [BA 10] PFC in the masked condition and the ventromedial [BA 10], ventrolateral [BA 47] PFC, and orbitofrontal [BA 11] cortex in the unmasked condition). It has been shown that the medial PFC is especially involved in the recognition of angry facial expression (Blair et al. 1999; Harmer et al. 2001). Our finding might indicate that sensitizers allocate more cognitive resources to the identification and analysis of a threatening stimulus than repressors when the potential threat indicates a direct risk for the health and safety of the observer. In response to unmasked angry faces, repressive individuals again exhibited an enhanced activation of visual processing areas compared with sensitizing subjects.
In case of unmasked happy facial expression, repressors manifested a stronger activation of the frontal cortex (i.e., BA 11) than sensitizers. Repressors compared with sensitizers also showed more activation of temporo-occipital visual systems to clearly visible happy faces.
In sum, we demonstrate neural correlates of coping style for threat in healthy individuals. A network comprising subcortical and frontal cortical areas known to be involved in the processing of threat-related information is affected. The amygdala, frontal, and temporo-occipital cortical areas appear to represent important brain structures in the neurobiological substrates of coping modes. It had been hypothesized that repressors should differ from sensitizers on automatic as well as controlled information processing levels by inhibiting the processing of threatening stimuli (Krohne 1978, 1993; Hock and Egloff 1998; Krohne et al. 2000). Our finding of a higher response of visual processing areas to threatening (and nonthreatening) faces in repression is not consistent with this assumption. Repressive individuals appear not to be characterized by a reduced sensory analysis of threatening social signals but according to our results they even manifest an enhanced visual processing of threatening facial expression but also of faces that signal safety and acceptance. The enhanced responsivity in temporo-occipital visual systems might indicate a greater reliance on posterior perceptual mechanisms for stimulus analysis in repression.
Activation differences between repressors and sensitizers in response to facial emotion were observed for subcortical, that is, amygdalar brain regions. The increased amygdala response here was specific for the sensitizer individuals and (unmasked) fearful stimuli. The amygdala is a central site for operations in the fear circuit including the elicitation of feelings and behaviors of fear (Panksepp 1998; Mineka and Öhman 2002). Because we did not assess peripheral activity it remains unclear whether sensitizers actually showed more psycho-physiological fear responses compared with repressors. There was, however, no evidence that sensitizing individuals were more engaged in examining the ambiguous threatening faces or, for example, more engaged in self and emotion regulation or strategy selection, that is, cognitive operations which are ascribed to frontal network structures, when confronted with fear faces. According to our results repressors are cortically more responsive to fearful (ambiguously threatening) and happy (nonthreatening) facial expression than sensitizers, whereas sensitizers demonstrate an enhanced responsivity in several prefrontal areas to angry faces (i.e., unambiguously threatening expressions).
Future studies have to examine whether the enhanced visual processing of facial expression in repression could be due to a stronger autonomic responsivity. As pointed out above, repressors demonstrate typically stronger physiological arousal than sensitizers when confronted with threatening stimuli. There is evidence from neuroimaging studies that peripheral physiological arousal is correlated with neural responses in several brain regions (Critchley, Corfield, et al. 2000, 2005). High physiological responsivity of repressors may result in an enhanced activation of brain areas involved in central autonomic control such as the anterior cingulate compared with sensitizers. In addition, there is evidence that heart rate increase evoked by viewing emotional stimuli is associated with activity in visual cortical areas, that is, fusiform and adjacent lingual gyrus, and superior temporal cortex (Lang et al. 1998; Critchley et al. 2005).
In our sample, sensitizers described themselves as more trait anxious as repressors. However, it is well known that repressors and sensitizers exhibit strong differences in the willingness to communicate anxiety-related thoughts and experiences to others. Therefore, one must be cautious in the interpretation of the (STAI) self-report data as indices of trait anxiety. Repressors tend to describe themselves as more adapted and less disturbed than they really are, whereas sensitizers tend to describe themselves as less adapted and more disturbed than they are (Krohne 1978; Hock et al. 1996).
Sander et al. (2003) found evidence that independent of task orbitofrontal cortical activation was larger for repressors than for nonrepressors in response to prosodic information. In Sander et al.'s study happy and sad intonations were presented. Overall, it appears that when confronted with not directly threatening emotional (i.e., fearful, sad, and happy) information repressors show stronger frontal cortical responses than sensitizers. The latter show stronger frontal activation in response to stimuli signaling risk of direct harm infliction. In this specific condition, sensitizing individuals could manifest an enhanced cognitive or "higher-order" processing of the threat information. This pattern of findings appears, however, not easily compatible with the hypothesis that sensitizers are especially characterized by a high responsivity to uncertainty regarding source and location of threat (Krohne 1993).
Certain limitations to the present investigation should be acknowledged. The generalizability of our conclusions is limited because the number of subjects studied was relatively small. In addition, our stimulus material was limited to facial expressions of emotions. As with any passive viewing paradigm, behavioral data were not collected. Future studies based on explicit emotion processing tasks may detect more distinct response patterns between repressors and sensitizers in prefrontal cortical areas because they are known to be especially activated by such tasks (Critchley, Daly, et al. 2000; Lange et al. 2003). Individual coping styles vary across a continuous spectrum and include both repressing and sensitizing components. As a first step, we chose to examine consistent repressors and consistent sensitizers. Our self-report data indicate that study participants were not very anxious during the fMRI experiment. The impact of a more severely threatening stimulation on brain activation in repression and sensitization therefore remains to be investigated. In the present study, only direct-gaze facial displays were presented. The findings of Adams et al. (2003) suggest that amygdala sensitivity to angry and fearful faces varies differentially as a function of eye gaze. It is an important task of future investigation on coping strategies to incorporate gaze direction in work on perception of threatening facial expression. Future neuroimaging studies in this field may also include recording patients' autonomic responses and/or eye movements during picture presentation to further extend our knowledge about the neurobiology of repression and sensitization coping styles.
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Conflict of Interest: None declared.
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