Inter-individual differences in the habitual use of cognitive reappraisal and expressive suppression are associated with variations in prefrontal cognitive control for emotional information: An event related fMRI study
Highlights
► Reappraisers are faster in disengaging from sad faces as compared to happy faces. ► Reappraisers show more DLPFC and dACC activation when disengaging from the negative. ► Suppressors show higher amygdala activation during disengagement from sad faces. ► Neural correlates of cognitive control are related to emotion regulation.
Introduction
It is a unique human ability to control our experience and expression of emotions, an ability known as emotion regulation. This ability allows us to control the variety of emotions we experience and facilitates how to express those feelings (Gross, 1998). Although there are many different strategies which influence our experience of emotion (Lazarus, 1991, Gross, 1998), we chose to examine two very different and well-established emotion regulation strategies (ERs): cognitive reappraisal and expressive suppression. Defined by Gross (1998), cognitive reappraisal is a means of changing the way one thinks about a potentially emotion eliciting situation in order to reduce its emotional impact. Expressive suppression, on the other hand, is a means of response modulation whereby an individual voluntarily inhibits emotional expressive behavior. These strategies are prototypical as to how humans control emotions in daily life (Ochsner and Gross, 2005).
In an attempt to explore the roots of differences in ERs, researchers have investigated the neural correlates of these higher order thinking styles. fMRI research has shown that the use of both ERs is highly correlated with neural activity in a prefrontal cortical system, including the dorsolateral prefrontal cortex (DLPFC), the dorsal parts of the anterior cingulate cortex (dACC) and the ventromedial prefrontal cortex (VMPFC) (e.g., Beauregard et al., 2001, Ochsner et al., 2002, Ochsner et al., 2004, Urry et al., 2006). Here, the degree of emotion regulation success was investigated as indexed by the change in negative affect and neural activity when reappraising or suppressing emotional images or film fragments. Another approach is to investigate individual differences in ER, exploring the influence of the habitual use of reappraisal and suppression on brain functioning. It has been reported that the habitual use of reappraisal (as measured with questionnaires) was associated with decreased amygdala activity, and increased prefrontal and parietal activity during the processing of negative emotional facial expressions, even after controlling for individual suppression scores (Drabant et al., 2009). Additionally, the habitual use of reappraisal has also been found to correlate positively with dACC volume (Giuliani et al., 2011a). On the other hand, the habitual use of expressive suppression has been associated with decreased activation of the orbital medial prefrontal cortex when negative pictures were expected to appear (Abler et al., 2010), and this tendency was also associated with increased baseline perfusion of the medial prefrontal cortex (Abler et al., 2008). Moreover, recently a positive relationship has been found between the habitual use of suppression and anterior insula volume (Giuliani et al., 2011b). To briefly summarize on this topic, the neural activation patterns associated with individual differences in ERs point towards an important role of fronto-cingulate regions.
Fronto-cingulate regions associated with ERs seem to be similarly activated during experimental tasks that measure cognitive control for emotional material (e.g., Fales et al., 2008, Etkin et al., 2006). In general, cognitive control relates to the ability to guide task performance by activating goal-directed behavior and inhibiting habitual response tendencies (Edwards et al., 2010, Banich et al., 2009). It might be that cognitive control processes are functional mechanisms underlying the use of higher order cognitive strategies to regulate emotions. Within this context, individual differences in the habitual use of cognitive reappraisal have been found to correlate positively with cognitive control to reduce errors (McRae et al., in press) and with increased cognitive control to inhibit the processing of negative information when using a negative priming paradigm (Joormann and Gotlib, 2010). The tendency to use expressive suppression was also found to be inversely correlated with cognitive control towards negatively loaded material (Joormann and Gotlib, 2010), and positively correlated with cognitive costs during memory tasks (Richards and Gross, 2000). These findings suggest an association between the habitual use of a specific ER and cognitive processes to control negative information. Although ERs and cognitive control rely on the same fronto-cingulate neural circuitries, this association has not yet been confirmed by neuroimaging data. Hence, the aim of the present study is to relate self-reported reappraisal and suppression tendencies to neural correlates of cognitive control processes for emotional information. Information on how specific underlying cognitive processes are related to suppression and reappraisal might increase our understanding of inter-individual differences in the habitual use of these ERs in everyday life. In our opinion this is highly relevant as habitual suppression is related to greater negative affect, whereas habitual reappraisal is related to higher wellbeing (Gross and John, 2003).
The cognitive control ability to inhibit prepotent responses in particular has been primarily investigated with emotional Stroop (e.g., Gotlib et al., 2005, Etkin et al., 2006) or affective interference tasks (Siegle et al., 2002, Fales et al., 2008). Although valuable, these paradigms are characterized by an important limitation: conflict and stimulus identity are both present within the same stimulus presentation. In the current study, cognitive control for emotional material was measured using the Cued Emotional Conflict Task in which emotional interference is based on the presentation of a prior cue (CECT; Fig. 1, Vanderhasselt et al., in press). On each CECT trial, a preparatory cue instructs participants to respond to the actual emotion or to the opposite emotion of an upcoming stimulus. Following a fixed interval after this cue, a happy or sad facial expression is presented on the screen and participants have to respond to this emotional target. In this way, the conflict during the presentation of the emotional target is dependent of the presentation of a prior cue (i.e., the conflict during the target is higher when the cue was “opposite” as compared to “actual”) and not on interfering emotional stimulus dimensions.
In short, the goal of this study is to associate neural correlates of cognitive control during the performance of the CECT with self-reported use of emotion regulation strategies. The habitual use of cognitive reappraisal and expressive suppression will be measured by the well validated Emotion Regulation Questionnaire (ERQ: Gross and John, 2003). Based on the current evidence (e.g., Joormann and Gotlib, 2010), we expected (1) that the habitual use of cognitive reappraisal would correlate positively, and (2) the habitual use of expressive suppression would correlate negatively with cognitive control processes for negative information. Using the CECT, cognitive control to inhibit a dominant response to negative information in favor of the opposite emotion (cue “opposite “followed by a sad face) will be measured. This process of maintaining goal-relevant information online in order to strategically attend to specific information in the environment has been related to activity in the DLPFC/dACC (Vanderhasselt et al., 2009b, De Raedt et al., 2010). Therefore, we expected that, during cognitive control for negative material, inter-individual differences in reappraisal and suppression scores would be related to activation in the DLPFC/dACC. Moreover, because the amygdala has an important role in responses to negative emotions (Phelps, 2006), we also expected a relationship with this subcortical region.
Section snippets
Participants
Internet postings were used to recruit 31 never depressed female participants with a mean age of 21.07 years (SD = 2.36, range 18–30). Participants were invited to the hospital for a Structured Clinical Interview for DSM-IV disorders (MINI; Sheehan et al., 1997), which was administered by a trained psychiatrist. Exclusion criteria were: (1) current or prior history of psychopathology; (2) a history of neurological conditions including loss of consciousness for more than 5 min; (3) substance abuse
Self-report data
The mean reappraisal score was 28.32 (SD = 4.61; [15–35]) and the mean suppression score was 11.52 (SD = 5.19; [5–22]). The internal consistencies of both subscales were good: Cronbach's alpha for cognitive reappraisal items is .80 and for expressive suppression items .84
Behavioral data
Overall, accuracy rates for all four CECT trial types were high (85–97.5%). A repeated measures ANOVA with Cue (Opposite, Actual) × Emotion (Sad, Happy) on RT revealed a main effect of Cue, F(1,29) = 155.07, p < .001, , due to
Discussion
The aim of this study was to investigate whether inter-individual differences in the habitual use of cognitive reappraisal and expressive suppression are related to processes of prefrontal cognitive control for emotional material. All participants were healthy and never depressed female volunteers.
First, across all participants, behavioral data indicated a positivity bias: faster RT to respond to positive information (actual-happy trials: response is happy), but longer RT to inhibit a dominant
Acknowledgements
MAV (FWO08/PDO/168) is a postdoctoral fellow of the Research Foundation Flanders (FWO). This research was also supported by a grant from the Scientific Fund W. Gepts UZ Brussel and by the Ghent University Multidisciplinary Research Partnership “The integrative neuroscience of behavioral control” (CB). Preparation of this paper was supported by Grant BOF10/GOA/014 for a Concerted Research Action of Ghent University (awarded to RDR). The authors want to thank Maud Grol for her assistance in
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