Emotional self-reference: Brain structures involved in the processing of words describing one's own emotions☆
Highlights
► Healthy participants read emotion words varying in self-reference. ► Emotion words were related to the self, the other or had no self-other reference. ► Brain activity was investigated by means of functional imaging methods. ► Processing of emotion words increased amygdala and insula activity. ► MPFC (vMPFC and ACC) were activated specifically for self-related emotion words.
Introduction
Emotion and the self are two fascinating research topics. Ever since William James, researchers have sought answers to the questions what constitutes emotions and the self and how both phenomena might interact. Although no clear theoretical consensus has yet been reached, contemporary empirical research converges on the view that both, emotion and the self, are neurally grounded phenomena (Damasio, 1994, Damasio, 1999), and associated with activity changes in specific brain regions. Regarding emotions, neuroimaging studies have been successful in tracing the brain circuitry underlying the processing of emotional stimuli. One robust finding of this research is that processing of emotional stimuli leads to enhanced activity in the amygdala. This could be demonstrated for different stimulus materials, including high arousing pictures, faces (Zald, 2003, for reviews) as well as more symbolic stimuli such as emotionally arousing words (e.g., Cunningham et al., 2004, Hamann and Mao, 2002, Herbert et al., 2009, Tabert et al., 2001). Although the amygdala responds rapidly to emotional information this does not mean that the subjects themselves actually experience fear or any emotion at all when looking at a photograph of a fearful face, or while reading an emotionally challenging word. In general emotions can be characterized as adaptive response patterns of an organism, associated with changes in the body and the brain, that are elicited instantaneously in the presence of emotionally significant external or internal events that promote or challenge the organisms survival and well-being (Russell, 2003, Scherer, 2005). These response patterns and concomitant changes in the body and the brain need not be consciously aware to the subject (Craig, 2008, Damasio, 1994, Damasio, 1999). Feelings might result from emotions, however in contrast to emotions, feelings refer to the subjective and conscious experience of emotions (e.g., Barrett et al., 2007a, Damasio, 1994, Damasio, 1999).
Lesion studies suggest that the amygdala is involved in more basic emotional processing, but not necessarily in conscious emotion processing and the generation of feelings (e.g., Adolphs et al., 1994, Anderson and Phelps, 2002; for reviews see Adolphs, 2002). The amygdala is an emotion detection structure (Damasio, 1994, Damasio, 1999, LeDoux, 1996, Öhman and Mineka, 2001). It ensures reflexive responding to stimuli that challenge or protect individual survival and well-being. Activation of the amygdala might therefore also change, and/or increase in intensity during processing of personally relevant emotional stimuli (Adolphs et al., 1998, Cristinzio et al., 2011, N’Diaye et al., 2010, Modinos et al., 2009, Rameson et al., 2010, Yoshimura et al., 2009). This would be in line with the suggestion that the amygdala responds to a broad range of stimuli of emotional significance and of subjective emotional relevance (Sander, Grandjean, & Scherer, 2005).
Regarding the self, several neuroimaging studies demonstrate specific brain regions to be more active when individuals engage in self-referential processing tasks like judging stimuli (e.g., trait adjectives) in terms of their personal relatedness or self-descriptiveness (Craik et al., 1999, Kelley et al., 2002, Zysset et al., 2003; for review see Northoff et al., 2006). Subcomponents of this so called cortical midline structures (CMS) comprise, in particular, the medial prefrontal cortex (MPFC), and, amongst others, the posterior cingulate cortex (PCC) and the inferior parietal cortex (e.g., the precuneus) (for reviews on CMS see Northoff & Bermpohl, 2004). Several studies report changes in activity in regions of the CMS during active emotional modulation tasks. Most of these studies used tasks, in which participants were explicitly instructed to evaluate the emotional stimuli for their self-descriptiveness, their personal relevance (e.g., like me vs. not like me), or from a first relative to a third person perspective (e.g., Fossati et al., 2003, Gusnard et al., 2001, Moran et al., 2006; for an overview see Lee & Siegle, 2009). Other tasks employed in these studies used active emotion regulation conditions during which participants actively regulated their responses to emotional stimuli by reappraising their meaning with regard to the implications for themselves (e.g., Ochsner et al., 2002, Ochsner et al., 2004a, Ochsner et al., 2004b).
One emerging point of evidence from these studies is that reflection upon the own emotional state enhances activity in the medial prefrontal cortex (MPFC). The MPFC is interconnected with dorsal prefrontal cortex, the anterior cingulate cortex (ACC) and the insular cortex and receives in- and output from limbic emotion structures such as the amygdala (Fuster, 2008), thus providing a converging zone for the integration of information about interoceptive sensations, cognitive and emotional states. Notably the ventral MPFC (vMPFC) is more engaged in the evaluation of own emotions compared to, for instance, the emotions of others or a control condition (e.g., passive viewing). The dorsal MPFC (dMPFC), in contrast, appears to be related to self-referential processing in general (Schmitz & Johnson, 2007). Models based on meta-analytical data regarding emotion and the self (Northoff and Bermpohl, 2004, Schmitz and Johnson, 2007) suggest two different medial prefrontal sub-systems: The first system primarily comprises the vMPFC, the anterior cingulate (ACC), amygdala and insula. This sub-system is hypothesized to be responsible for the online evaluation of incoming emotional information as self-relevant. The second sub-system, including the dMPFC, precuneus and posterior cingulate cortex, is supposed to enable a more detailed stimulus analysis based on self-reflection either in conjunction with or independent of the former sub-system. Up to now, it remains unclear if changes in activity in one or both of these MPFC systems can be stimulated by self-related emotional stimuli in the absence of presented self-reflective processing instructions.
Research on embodied cognition (e.g., Barrett and Lindquist, 2008, Barrett et al., 2007b), as well as traditional semantic network models of emotion and cognition (Bower, 1981, Lang, 1979) suggest that processing of emotional content encompasses links to all aspects of its perceptual properties, its usage and emotional connotations. Thus, the word fear, for example, not only represents the concept of fear, but includes links to the word's purpose, operations and physiological consequences, possibly reinstating feelings of pleasure/displeasure and arousal even in the absence of a concrete emotion eliciting external event. This has also been highlighted by emotion models stating the relevance of the representation of actual and reactivated bodily experiences (Craig, 2002, Craig, 2009, Damasio, 1994, Damasio, 1999). Reading verbal expressions describing own emotions might thus automatically arouse and activate the amygdala, and additionally direct the reader's attention towards the monitoring of internal, mental and bodily states and the evaluation of emotional experience from current and past experience.
Previous research suggest that both the vMPFC, the insula and the ACC are key structures associated with subjective awareness of inner bodily states (interoception) and the representation and regulation of subjective emotional experience (Barrett et al., 2007a, Craig, 2002, Craig, 2009, Lane, 2000, Paulus and Frank, 2003, Zysset et al., 2003). Accordingly, one would expect activity in the amygdala, insula but also the MPFC (vMPFC in particular) and the ACC to be more active during processing of words related the own emotion compared to a control condition of passive viewing of emotion words that contain no particular reference or are related to another person.
Building upon and extending previous research the present study aimed, for the first time, to directly investigate this hypothesis by measuring brain activity underlying the processing of one's own emotions without confounding effects related to a specific task at hand. To this end, healthy participants underwent functional imaging while they read silently a series of verbal expressions that described either own emotions, the emotions of another person or contained no self-other reference at all.
Section snippets
Participants
Twenty-two healthy, right-handed native speakers of German (eight males, fourteen females; mean age: 23.5 years, SD = 2.7) without history of drug abuse, chronic bodily or neurological and psychiatric diseases, or medication for any of these participated in the fMRI experiment. All participants scored normally on self-report measures of mood (M = 3.3; SD = 2.5) (BDI, Hautzinger, Bailer, Worall, & Keller, 1194), and also state (M = 35.7; SD = 5.3) and trait anxiety (M = 36.3; SD = 5.8) (STAI, Laux, Glanzmann,
Effects of emotion, unreferenced
Activity in the left amygdala as well as the right insula was significantly enhanced during reading of unpleasant compared to neutral nouns that contained no self-other reference (Table 1a). For pleasant nouns, there was no difference in amygdala or insula activity compared to neutral nouns. Also, there was a significant increase in activity in occipital, parietal as well as temporal brain regions during reading of emotional (unpleasant and unpleasant) compared to neutral nouns (Table 1b).
Effects of self-reference on emotion processing
Discussion
The present study demonstrates how variations in stimulus reference (related to the self, vs. the other, vs. no particular reference) associated with emotion words influence brain activity patterns in emotion-related and self-related brain structures in a silent reading task. During reading, processing of unpleasant words compared to neutral and pleasant words increased amygdala and insula activation regardless of the stimuli's reference (self, other, no reference). This is consistent with
Acknowledgements
This research study was supported by the German Research Foundation (DFG).
We thank the reviewers and the Editor Daniel T. Tranel for their helpful comments on our manuscript.
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2020, Neuroscience and Biobehavioral ReviewsCitation Excerpt :In particular, “transforming” subjective feelings into words may not only induce emotions and feeling states, but may also modulate emotion perception (Barrett et al., 2016; Herbert et al., 2013; Lindquist et al., 2015). Interestingly, reading words that refer to the reader’s own emotions has been found to elicit changes in neural activity in the left and right insula, amygdala, and parts of the ventral medial prefrontal cortex (Herbert et al., 2011), all known to be critically involved in the awareness of body states (interoception), in self-referential processing of emotions and in feelings of emotional ownership (Northoff et al., 2006). The meta-analysis conducted within this review (see section 5) supports an overlap of activation in dedicated brain regions for language and affective feelings including the insula.
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2018, Trends in Cognitive SciencesCitation Excerpt :We propose here that emotional or self-referential information engages overlapping processes that are beneficial to memory encoding (see Glossary), increasing the likelihood that information is retained in memory. Many before us have written about the overlap between the experience of emotion and self-relevance (e.g., [8–11]). It is hard to envisage real-world scenarios in which emotion is elicited but the event contains no self-importance, and some theories of emotion dictate that self-relevance must be present for emotion to arise (e.g., [12]).
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The complete list of the words used in this study (original and translation) is available from the authors upon request.